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Bacterial flagella: twist and stick, or dodge across the kingdoms.

Rossez Y, Wolfson EB, Holmes A, Gally DL, Holden NJ - PLoS Pathog. (2015)

Bottom Line: An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components.At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms.These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

View Article: PubMed Central - PubMed

Affiliation: Cellular and Molecular Sciences, James Hutton Institute, Dundee, United Kingdom.

ABSTRACT
The flagellum organelle is an intricate multiprotein assembly best known for its rotational propulsion of bacteria. However, recent studies have expanded our knowledge of other functions in pathogenic contexts, particularly adherence and immune modulation, e.g., for Salmonella enterica, Campylobacter jejuni, Pseudomonas aeruginosa, and Escherichia coli. Flagella-mediated adherence is important in host colonisation for several plant and animal pathogens, but the specific interactions that promote flagella binding to such diverse host tissues has remained elusive. Recent work has shown that the organelles act like probes that find favourable surface topologies to initiate binding. An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components. At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms. Bacteria have evolved different strategies to evade or even promote this specific recognition, with some important differences shown for phytopathogens. These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

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Cross-kingdom immune recognition of flagellin structures.Top: backbone of the key residues of flagellin recognized by plant (left) and animal (right) innate immune receptors are highlighted in red. FliC from S. enterica is presented as a “model” flagellin, with reports for recognition by both TLR5 and FLS2 receptors. These residues are superimposed on the solved flagellin structure (PDB# 1UCU) in UCSF Chimera [113]. Surfaces and backbone are coloured according to previously assigned structural domains as indicated below each monomer [57]. Bottom: recognition of flagella filaments by plant (left) and animal (right) innate immune receptors does not occur as key residues (surfaces highlighted in red) are hidden within the filament structure. However, immune recognition still occurs in animals via antibody recognition of the D3 domain.
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ppat.1004483.g002: Cross-kingdom immune recognition of flagellin structures.Top: backbone of the key residues of flagellin recognized by plant (left) and animal (right) innate immune receptors are highlighted in red. FliC from S. enterica is presented as a “model” flagellin, with reports for recognition by both TLR5 and FLS2 receptors. These residues are superimposed on the solved flagellin structure (PDB# 1UCU) in UCSF Chimera [113]. Surfaces and backbone are coloured according to previously assigned structural domains as indicated below each monomer [57]. Bottom: recognition of flagella filaments by plant (left) and animal (right) innate immune receptors does not occur as key residues (surfaces highlighted in red) are hidden within the filament structure. However, immune recognition still occurs in animals via antibody recognition of the D3 domain.

Mentions: The flagellin monomer is organised into four connected domains designated D0, D1, D2, and D3 (Fig. 2) [57]. To form these domains, flagellin peptides fold back on themselves, like an elaborate hairpin, with the termini associated with one another. The D2–D3 domains are highly variable and generate the antigenic diversity described as H-serotypes [58–60]. The termini that form the D0–D1 domains are well conserved across all bacterial flagellins. Both N- and C-termini are rich in hydrophobic residues, which form coiled–coil interfaces that allow them to associate with one another; these interfaces are also required for filament polymerisation [3,61,62]. Importantly, the flagellin needs to be disassociated to make D0–D1 accessible to innate immune receptors, in contrast to the polymeric structure involved in binding interactions. Flagellin recognition occurs in plant cells [63] and animal cells of both invertebrates [64] and vertebrates [65]. The receptors for these conserved regions are Toll-like receptor 5 (TLR5) for extracellular flagellin [66–68] and NAIP5-NLRC4 for intracellular flagellin [69] in vivo, and Flagellin sensitive 2 (FLS2) receptor for flagellin in planta (Fig. 2) [70].


Bacterial flagella: twist and stick, or dodge across the kingdoms.

Rossez Y, Wolfson EB, Holmes A, Gally DL, Holden NJ - PLoS Pathog. (2015)

Cross-kingdom immune recognition of flagellin structures.Top: backbone of the key residues of flagellin recognized by plant (left) and animal (right) innate immune receptors are highlighted in red. FliC from S. enterica is presented as a “model” flagellin, with reports for recognition by both TLR5 and FLS2 receptors. These residues are superimposed on the solved flagellin structure (PDB# 1UCU) in UCSF Chimera [113]. Surfaces and backbone are coloured according to previously assigned structural domains as indicated below each monomer [57]. Bottom: recognition of flagella filaments by plant (left) and animal (right) innate immune receptors does not occur as key residues (surfaces highlighted in red) are hidden within the filament structure. However, immune recognition still occurs in animals via antibody recognition of the D3 domain.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4295861&req=5

ppat.1004483.g002: Cross-kingdom immune recognition of flagellin structures.Top: backbone of the key residues of flagellin recognized by plant (left) and animal (right) innate immune receptors are highlighted in red. FliC from S. enterica is presented as a “model” flagellin, with reports for recognition by both TLR5 and FLS2 receptors. These residues are superimposed on the solved flagellin structure (PDB# 1UCU) in UCSF Chimera [113]. Surfaces and backbone are coloured according to previously assigned structural domains as indicated below each monomer [57]. Bottom: recognition of flagella filaments by plant (left) and animal (right) innate immune receptors does not occur as key residues (surfaces highlighted in red) are hidden within the filament structure. However, immune recognition still occurs in animals via antibody recognition of the D3 domain.
Mentions: The flagellin monomer is organised into four connected domains designated D0, D1, D2, and D3 (Fig. 2) [57]. To form these domains, flagellin peptides fold back on themselves, like an elaborate hairpin, with the termini associated with one another. The D2–D3 domains are highly variable and generate the antigenic diversity described as H-serotypes [58–60]. The termini that form the D0–D1 domains are well conserved across all bacterial flagellins. Both N- and C-termini are rich in hydrophobic residues, which form coiled–coil interfaces that allow them to associate with one another; these interfaces are also required for filament polymerisation [3,61,62]. Importantly, the flagellin needs to be disassociated to make D0–D1 accessible to innate immune receptors, in contrast to the polymeric structure involved in binding interactions. Flagellin recognition occurs in plant cells [63] and animal cells of both invertebrates [64] and vertebrates [65]. The receptors for these conserved regions are Toll-like receptor 5 (TLR5) for extracellular flagellin [66–68] and NAIP5-NLRC4 for intracellular flagellin [69] in vivo, and Flagellin sensitive 2 (FLS2) receptor for flagellin in planta (Fig. 2) [70].

Bottom Line: An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components.At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms.These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

View Article: PubMed Central - PubMed

Affiliation: Cellular and Molecular Sciences, James Hutton Institute, Dundee, United Kingdom.

ABSTRACT
The flagellum organelle is an intricate multiprotein assembly best known for its rotational propulsion of bacteria. However, recent studies have expanded our knowledge of other functions in pathogenic contexts, particularly adherence and immune modulation, e.g., for Salmonella enterica, Campylobacter jejuni, Pseudomonas aeruginosa, and Escherichia coli. Flagella-mediated adherence is important in host colonisation for several plant and animal pathogens, but the specific interactions that promote flagella binding to such diverse host tissues has remained elusive. Recent work has shown that the organelles act like probes that find favourable surface topologies to initiate binding. An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components. At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms. Bacteria have evolved different strategies to evade or even promote this specific recognition, with some important differences shown for phytopathogens. These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

Show MeSH
Related in: MedlinePlus