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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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A variety of mechanisms employed to “dodge” the flagellin innate immune response.(A) Flagella filaments degrade, releasing monomeric flagellin, the residues of which are recognised by receptor TLR5, NLRC4, or FLS2, resulting in cytokine release or PTI. The example residues and receptor (right) shown are involved in TLR5 recognition. (B) Flagellin recognition by TLR5, NLRC4, or FLS2 is evaded by variation in key residues involved in flagellin detection, which can necessitate compensatory mutations. (C) Bacteria secrete enzymes that specifically target and degrade monomeric flagellin, preventing its recognition by TLR5, NLRC4, or FLS2. (D) Post-translational glyosylation of flagellin is thought to enhance flagella stability; reduced release of flagellin from flagella filaments will result in reduced recognition by TLR5 or FLS2. (E) Bacteria secrete effector proteins that interfere with TLR5, NLRC4, or FLS2 recognition either by direct inhibition of receptor expression or binding, or by inhibition of downstream signalling pathways. (F) Bacteria down-regulate or switch off flagella expression when motility and/or binding are no longer required.
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ppat.1004483.g003: A variety of mechanisms employed to “dodge” the flagellin innate immune response.(A) Flagella filaments degrade, releasing monomeric flagellin, the residues of which are recognised by receptor TLR5, NLRC4, or FLS2, resulting in cytokine release or PTI. The example residues and receptor (right) shown are involved in TLR5 recognition. (B) Flagellin recognition by TLR5, NLRC4, or FLS2 is evaded by variation in key residues involved in flagellin detection, which can necessitate compensatory mutations. (C) Bacteria secrete enzymes that specifically target and degrade monomeric flagellin, preventing its recognition by TLR5, NLRC4, or FLS2. (D) Post-translational glyosylation of flagellin is thought to enhance flagella stability; reduced release of flagellin from flagella filaments will result in reduced recognition by TLR5 or FLS2. (E) Bacteria secrete effector proteins that interfere with TLR5, NLRC4, or FLS2 recognition either by direct inhibition of receptor expression or binding, or by inhibition of downstream signalling pathways. (F) Bacteria down-regulate or switch off flagella expression when motility and/or binding are no longer required.

Mentions: Since flagellin is such an important immunogen, bacteria have evolved multiple strategies to avoid or evade recognition (Fig. 3). Some pathogens enocode multiple flagellin types, which may relate to evasion or even niche versatility [81]. The majority of S. enterica encode two flagellin types (phase 1 & 2), under phase variable control of expression [81–84]. A third flagellin gene, flpA, has also been described for a particular S. enterica isolate [84]. However, control of expression may be of greater importance in evasion. Nonflagellate mutants out-competed flagellated EHEC O157:H7 colonisation in cattle [85], and nonflagellated strains of plant pathogens Xanthomonas fuscans subsp. fuscans are isolated from natural epidemics of plant disease [86]. Furthermore, attenuation of infection occurred when phase 2 flagella were constitutively expressed in S. Tyhimurium, following oral or intravenous inoculation of mice were in the mouse model of infection [87].


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

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

A variety of mechanisms employed to “dodge” the flagellin innate immune response.(A) Flagella filaments degrade, releasing monomeric flagellin, the residues of which are recognised by receptor TLR5, NLRC4, or FLS2, resulting in cytokine release or PTI. The example residues and receptor (right) shown are involved in TLR5 recognition. (B) Flagellin recognition by TLR5, NLRC4, or FLS2 is evaded by variation in key residues involved in flagellin detection, which can necessitate compensatory mutations. (C) Bacteria secrete enzymes that specifically target and degrade monomeric flagellin, preventing its recognition by TLR5, NLRC4, or FLS2. (D) Post-translational glyosylation of flagellin is thought to enhance flagella stability; reduced release of flagellin from flagella filaments will result in reduced recognition by TLR5 or FLS2. (E) Bacteria secrete effector proteins that interfere with TLR5, NLRC4, or FLS2 recognition either by direct inhibition of receptor expression or binding, or by inhibition of downstream signalling pathways. (F) Bacteria down-regulate or switch off flagella expression when motility and/or binding are no longer required.
© Copyright Policy
Related In: Results  -  Collection

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

ppat.1004483.g003: A variety of mechanisms employed to “dodge” the flagellin innate immune response.(A) Flagella filaments degrade, releasing monomeric flagellin, the residues of which are recognised by receptor TLR5, NLRC4, or FLS2, resulting in cytokine release or PTI. The example residues and receptor (right) shown are involved in TLR5 recognition. (B) Flagellin recognition by TLR5, NLRC4, or FLS2 is evaded by variation in key residues involved in flagellin detection, which can necessitate compensatory mutations. (C) Bacteria secrete enzymes that specifically target and degrade monomeric flagellin, preventing its recognition by TLR5, NLRC4, or FLS2. (D) Post-translational glyosylation of flagellin is thought to enhance flagella stability; reduced release of flagellin from flagella filaments will result in reduced recognition by TLR5 or FLS2. (E) Bacteria secrete effector proteins that interfere with TLR5, NLRC4, or FLS2 recognition either by direct inhibition of receptor expression or binding, or by inhibition of downstream signalling pathways. (F) Bacteria down-regulate or switch off flagella expression when motility and/or binding are no longer required.
Mentions: Since flagellin is such an important immunogen, bacteria have evolved multiple strategies to avoid or evade recognition (Fig. 3). Some pathogens enocode multiple flagellin types, which may relate to evasion or even niche versatility [81]. The majority of S. enterica encode two flagellin types (phase 1 & 2), under phase variable control of expression [81–84]. A third flagellin gene, flpA, has also been described for a particular S. enterica isolate [84]. However, control of expression may be of greater importance in evasion. Nonflagellate mutants out-competed flagellated EHEC O157:H7 colonisation in cattle [85], and nonflagellated strains of plant pathogens Xanthomonas fuscans subsp. fuscans are isolated from natural epidemics of plant disease [86]. Furthermore, attenuation of infection occurred when phase 2 flagella were constitutively expressed in S. Tyhimurium, following oral or intravenous inoculation of mice were in the mouse model of infection [87].

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