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Chapter 27 : Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections

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Abstract:

The discovery of penicillin in 1928 and its subsequent introduction as a therapeutic in the 1940s sparked the antibiotic era, ushering in effective treatment options for many common bacterial infections ( ). Following the end of World War II, several pharmaceutical companies including Bayer, Merck, and Pfizer became household names through the discovery and clinical success of a number of additional antibiotics, which were identified by screening soil samples for antimicrobial activity ( ). Compounds identified during this screening became the founding members of many now-ubiquitous groups of antibiotics, including the tetracycline, rifamycin, quinolone, and aminoglycoside families. In the early 1970s, declining rates of novel antibiotic discovery from microbial sources shifted the onus of antimicrobial development to synthetic chemists, who were tasked with designing and screening new compounds based on known principles of antibiotic design. These synthetic chemists were faced with many practical challenges, including poor penetration into bacterial cells, bacterial enzymes, and/or efflux pumps that degrade or expel the compounds, respectively, innate resistance mechanisms, and the requirement of high concentrations of some compounds that result in toxic side effects ( ).

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Figures

Image of Figure 1
Figure 1

Comparison of structure and assembly mechanism of common extracellular adhesive organelles. Following translocation through the SecYEG apparatus, the FimA structural subunits are bound by the FimC chaperone via the donor strand complementation reaction before delivery to the FimD usher, which catalyzes a donor strand exchange reaction that links subunits of the growing pilus. In the periplasmic space, soluble CsgA binds the CsgE chaperone, which delivers it to the CsgG pore for secretion to the outer membrane. From there, its folding and polymerization is nucleated by CsgB, which is anchored to the outer membrane by the CsgF assembly factor. Ebp pilus subunits integrate themselves into the membrane, where the dedicated pilus assembly sortase, SrtC, cleaves the sorting sequence and facilitates the nucleophilic attack by a new incoming subunit. The fully assembled pilus is then integrated into the membrane by the housekeeping sortase, SrtA.

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Image of Figure 2
Figure 2

Inhibitors of the donor strand exchange reaction between pilus subunits are able to abrogate pilus biogenesis. Crystal structure of the FimG adaptor’s donor strand exchange reaction with the pilin domain of the FimH adhesin (PDB ID code 3JWN). FimG donates its hydrophobic N-terminal beta strand to FimH, which is shown residing in the P5 pocket. Schematic of the donor strand complementation and donor strand exchange pathways. The donor strand complementation reaction between the chaperone G1 strand and the bound pilin results in a noncanonical parallel fashion (left panel), while the zip-in, zip-out process underlying the DSE reactions results in the formation of an antiparallel, low-energy interaction (adapted from reference ). Chemical structure of compound 3, first identified from an docking assay before further refinement in DSE assays.

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Image of Figure 3
Figure 3

Small molecules known as “pilicides” disrupt pilus biogenesis. Structures of two potent curlicides. Curlicide 1 disrupts type 1, P, and S pili. Curlicide 2 binds to the P pilus chaperone PapD, inhibiting its interaction with the PapC usher. Electron micrographs demonstrating a loss of P pili on uropathogenic cells exposed to increasing concentrations of curlicide 2 (adapted from reference , with permission; copyright [2006] National Academy of Sciences, USA). Crystal structure of the two-domain adhesin FimH complexed with pilicide (PDB ID code 2J7L).

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Image of Figure 4
Figure 4

Curlicides inhibit biofilm formation. Structure of the curlicide 4 compound. Curlicide compounds are based on 2-pyridine scaffold functionalized with a variety of substituents. Inhibition of extracellular curli formation in the presence of increasing concentrations of curlicide 4 (adapted from reference ).

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Image of Figure 5
Figure 5

Potent inhibitors of sortase A function. X-ray crystal structure of sortase A from (PDB ID code 2KID) with docking of compound 5, which binds directly to the active site of the enzyme (adapted from reference , with permission). Structure of the sortase inhibitor compound 5, which inhibits sortase A from with an IC of 9.3 μM and with an IC of 0.82 μM.

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Image of Figure 6
Figure 6

Mannosides are potent inhibitors of FimH binding. Crystal structure of FimH complexed with mannoside 8, which binds to FimH with an affinity over 1 million times higher than its natural substrate, -mannose (PDB ID code 3MCY). Structure of a variety of mannosides, each rationally designed to increase affinity for FimH by interacting with the hydrophobic ridge outside of the mannose-binding pocket. Although heptyl α--mannoside 6 successfully bound FimH with a 600 times increased affinity when compared to -mannoside, the biphenyl substituents ultimately proved to be the most effective compounds (7, 8, and 9).

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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Image of Figure 7
Figure 7

Inhibitors of soluble lectins LecA and LecB. Structural depiction of the tetravalent calixarene scaffold, which can be functionalized with galactose and fucose moieties using triethylene glycol linkers to form compounds 11 and 10, respectively. Monovalent inhibitor of LecA 12 binds with a K of 4.2 μM. Monovalent inhibitor of LecB 13 activity binds with a K of 3.3 μM.

Citation: Cusumano Z, Klein R, Hultgren S. 2016. Innovative Solutions to Sticky Situations: Antiadhesive Strategies for Treating Bacterial Infections, p 753-795. In Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B (ed),

Virulence Mechanisms of Bacterial Pathogens, Fifth Edition

. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.VMBF-0023-2015
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