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Progress Overview of Bacterial Two-Component Regulatory Systems As Potential Targets for Antimicrobial Chemotherapy

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Progress Overview of Bacterial Two-Component Regulatory Systems As Potential Targets for Antimicrobial Chemotherapy antibiotics Review Progress Overview of Bacterial Two-Component Regulatory Systems as Potential Targets for Antimicrobial Chemotherapy Hidetada Hirakawa 1,*, Jun Kurushima 1, Yusuke Hashimoto 1 and Haruyoshi Tomita 1,2 1 Department of Bacteriology, Graduate School of Medicine, Gunma University, Maebashi Gunma 371-8511, Japan; [email protected] (J.K.); [email protected] (Y.H.); [email protected] (H.T.) 2 Laboratory of Bacterial Drug Resistance, Graduate School of Medicine, Gunma University, Maebashi Gunma 371-8511, Japan * Correspondence: [email protected] Received: 26 August 2020; Accepted: 21 September 2020; Published: 23 September 2020 Abstract: Bacteria adapt to changes in their environment using a mechanism known as the two-component regulatory system (TCS) (also called “two-component signal transduction system” or “two-component system”). It comprises a pair of at least two proteins, namely the sensor kinase and the response regulator. The former senses external stimuli while the latter alters the expression profile of bacterial genes for survival and adaptation. Although the first TCS was discovered and characterized in a non-pathogenic laboratory strain of Escherichia coli, it has been recognized that all bacteria, including pathogens, use this mechanism. Some TCSs are essential for cell growth and fitness, while others are associated with the induction of virulence and drug resistance/tolerance. Therefore, the TCS is proposed as a potential target for antimicrobial chemotherapy. This concept is based on the inhibition of bacterial growth with the substances acting like conventional antibiotics in some cases. Alternatively, TCS targeting may reduce the burden of bacterial virulence and drug resistance/tolerance, without causing cell death. Therefore, this approach may aid in the development of antimicrobial therapeutic strategies for refractory infections caused by multi-drug resistant (MDR) pathogens. Herein, we review the progress of TCS inhibitors based on natural and synthetic compounds. Keywords: two-component regulatory system; virulence; drug resistance; infection control; environmental response and adaptation; histidine kinase; response regulator 1. Introduction The shortage of antimicrobial agents caused by the increasing resistance of bacterial pathogens to current antibiotics is a severe concern in clinical settings. It is estimated that ten million people will die of drug-resistant infections in 2050 if this shortage is not solved [1]. The most commonly used antibiotics were introduced in the twenty years that followed the discovery of penicillin, and their widespread application has resulted in the development of drug-resistant bacteria. Therefore, there is a need to develop new classes of antibiotics, but the process is a challenging one. The two-component regulatory system (TCS) constitutes a system that enables bacteria to adapt to diverse environmental changes. This system is ubiquitous in bacteria, including animal and plant pathogens, but it is not present in mammalian cells, although some eukaryotic cells, such as fungi, yeast and several higher plant cells, including Arabidopsis thaliana, possess similar systems [2,3]. There are many reports that TCSs are associated with bacterial pathogenesis and/or drug resistance/tolerance in addition to fitness in a particular environment [4,5]. Additionally, some TCSs Antibiotics 2020, 9, 635; doi:10.3390/antibiotics9100635 www.mdpi.com/journal/antibiotics Antibiotics 2020, 9, 635 2 of 15 are needed for bacterial cell growth and survival [6–10]. Therefore, these systems have been proposed as potential targets for the development of antibacterial agents. The TCSAntibiotics essentially 2020, 9, x FOR comprises PEER REVIEW two types of proteins, termed “the sensor kinase”2 of (also15 called “the histidine kinase”) and “the response regulator” [11,12]. In signal transduction, the kinase senses an resistance/tolerance in addition to fitness in a particular environment [4,5]. Additionally, some TCSs external stimulus,are needed such for bacterial as a change cell growth in nutrient and survival levels, [6–10]. osmotic Therefore, pressure, these systems pH, redox have state,been proposed particular signal molecules,as antibiotics potential targets or membrane for the development stress. Afterward, of antibacterial a conserved agents. histidine residue in the sensor kinase is phosphorylated,The TCS followed essentially by comprises the transfer two oftypes the of phosphate proteins, termed group “the to asensor conserved kinase” aspartate(also calledresidue in the cognate“the response histidine regulator kinase”) and [11 “the]. Sensorresponse kinases regulator” are [11,12]. transmembrane In signal transduction, proteins the (mostly kinase senses homodimers) an external stimulus, such as a change in nutrient levels, osmotic pressure, pH, redox state, particular that exhibitsignal auto-phosphorylation molecules, antibiotics or and membrane phosphotransferase stress. Afterward, activities a conserved [13 ].histidine Consequently, residue in thethe response regulatorssensor demonstrate kinase is phosph conformationalorylated, followed changes by the when transfer phosphorylated, of the phosphate group then to thea conserved helix-turn-helix (HTH) domainaspartate dimer residue in in the the regulator cognate response protein regulato bindsr [11]. to aSensor target kinases DNA are region transmembrane adjacent proteins to a promoter. Afterward,(mostly the regulator homodimers) alters that the exhibit gene expressionauto-phosphorylation profiles byand modulatingphosphotransferase the activity activities of [13]. the promoter. Consequently, the response regulators demonstrate conformational changes when phosphorylated, Some sensorthen kinases the helix-turn-helix also exhibit (HTH) phosphatase domain dimer activity in the regulator in the absence protein binds of a signalto a target and DNA de-phosphorylate region response regulatorsadjacent to a (the promoter. schematic Afterward, diagram the regulator is shown alters in the Figure gene expression1)[ 14,15 profiles]. In 1992, by modulating unsaturated fatty acids, suchthe as activity oleic of acid, the promoter. were reported Some sensor to kinases attenuate also exhibit TCS activity phosphatase [16 ].activity These in the natural absence compounds of inhibited thea signal auto-phosphorylation and de-phosphorylate response of the sensor regulators kinase (the KinA,schematic which diagram is associatedis shown in Figure with sporulation1) [14,15]. In 1992, unsaturated fatty acids, such as oleic acid, were reported to attenuate TCS activity induction in[16].Bacillus These natural subtilis compounds. The first inhibited synthetic the auto-pho inhibitorssphorylation were reported of the sensor in 1993 kinase and KinA, targeted which a TCS of Pseudomonasis associated aeruginosa with(the sporulation following induction section in addressesBacillus subtilis how. The these first synthetic compounds inhibitors impair were TCSreported activity) [17]. Since the firstin 1993 study, and targeted a variety a TCS of of TCS Pseudomonas inhibitors aeruginosa have (the been following described section (summarized addresses how inthese Table A1 in the AppendixcompoundsA, and impair chemical TCS activity) structures [17]. ofSince representative the first study, inhibitorsa variety of areTCS drawninhibitors in have Figures been 2 and3). described (summarized in Table A1 in the Appendix A, and chemical structures of representative These compoundsinhibitors couldare drawn disrupt in Figures the TCS2 and through 3). These severalcompounds mechanisms could disrupt which the TCS include: through (1)several inhibition of sensor kinasemechanisms activity, which (2) inhibition include: (1) of inhibition response of regulatorsensor kinase activity, activity, (3) (2) sequestration inhibition of response of signal and (4) inhibitionregulator of signal activity, generation. (3) sequestration In the followingof signal and sections,(4) inhibition we of willsignal discuss generation. the In progress the following made in the developmentsections, of TCS we will inhibitors discuss the and progress also address made in th theire development properties. of TCS inhibitors and also address their properties. Figure 1. Two-componentFigure 1. Two-component regulatory regulatory system system (TCS) (TCS) in bacteria. in bacteria. When When the the membrane-bound membrane-bound homo- homo-dimeric dimeric sensor kinase senses a particular environmental stimulus, the conserved histidine residue (H) sensor kinase senses a particular environmental stimulus, the conserved histidine residue (H) in in the cytoplasmic sensor domain of this protein is phosphorylated (P) (termed auto-phosphorylation), the cytoplasmicthen transfers sensor its domain phosphate of group this proteinto the conserved is phosphorylated aspartate residue (P) (D) (termed in the receiver auto-phosphorylation), domain of then transfersthe cognate its phosphate response regulator. groupto The the kinase conserved activity depends aspartate on ATP residue which (D)is bound in the to the receiver catalytic domain of the cognate response regulator. The kinase activity depends on ATP which is bound to the catalytic domain (CA). The phosphorylated response regulator forms a homo-dimer, then the helix-turn-helix domain (HTH) of the response regulator binds to particular DNA sequences on or close to the promoter of target genes. Antibiotics 2020, 9, x FOR PEER REVIEW 3 of 15 domain (CA).
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