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Unexpected Enhancement of Antimicrobial Polymer Activity Against Staphylococcus Aureus in the Presence of Fetal Bovine Serum

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Unexpected Enhancement of Antimicrobial Polymer Activity Against Staphylococcus Aureus in the Presence of Fetal Bovine Serum molecules Communication Unexpected Enhancement of Antimicrobial Polymer Activity against Staphylococcus aureus in the Presence of Fetal Bovine Serum Iva Sovadinová 1 , Kenichi Kuroda 2,* and Edmund F. Palermo 3,* 1 RECETOX, Faculty of Science, Masaryk University, Kamenice 3, CZ-62500 Brno, Czech Republic; [email protected] 2 Department of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor, MI 48109, USA 3 Materials Science and Engineering, Rensselaer Polytechnic Institute, Troy, NY 12180, USA * Correspondence: [email protected] (K.K.); [email protected] (E.F.P.) Abstract: Cationic and amphiphilic polymers are known to exert broad-spectrum antibacterial activ- ity by a putative mechanism of membrane disruption. Typically, nonspecific binding to hydrophobic components of the complex biological milieu, such as globular proteins, is considered a deterrent to the successful application of such polymers. To evaluate the extent to which serum deactivates an- tibacterial polymethacrylates, we compared their minimum inhibitory concentrations in the presence and absence of fetal bovine serum. Surprisingly, we discovered that the addition of fetal bovine serum (FBS) to the assay media in fact enhances the antimicrobial activity of polymers against Gram-positive bacteria S. aureus, whereas the opposite is the case for Gram-negative E. coli. Here, we present these Citation: Sovadinová, I.; Kuroda, K.; unexpected trends and develop a hypothesis to potentially explain this unusual phenomenon. Palermo, E.F. Unexpected Enhancement of Antimicrobial Keywords: antimicrobial; polymer; S. aureus; serum Polymer Activity against Staphylococcus aureus in the Presence of Fetal Bovine Serum. Molecules 2021, 26, 4512. https://doi.org/10.3390/ 1. Introduction molecules26154512 The emergence of antibiotic multidrug-resistant bacterial infections has significantly complicated treatment, which presents a looming threat to public health worldwide [1]. To Academic Editors: Bruce P. Lee and address this critical challenge, cationic amphiphilic copolymers were designed to mimic Bo Liu host-defence antimicrobial peptides (AMPs) that act by compromising the barrier function of bacterial cell membranes [2–4]. AMP-mimetic copolymers show a broad spectrum of ac- Received: 14 June 2021 tivity, rapid bactericidal action, and low propensity to induce resistance, which collectively Accepted: 20 July 2021 Published: 27 July 2021 represent the hallmarks of AMP activity [5]. This polymer-based approach is expected to provide new robust and effective antimicrobials to eradicate drug-resistant bacteria. Indeed, S. aureus Publisher’s Note: MDPI stays neutral cationic polymethacrylates showed promising results in a mouse model of nasal with regard to jurisdictional claims in infection [6]. However, AMPs and AMP-mimetics often suffer from nonspecific binding to published maps and institutional affil- proteins, which significantly reduces their antimicrobial efficacy in the physiological milieu iations. such as blood, saliva, and other body fluids [7,8]. This key drawback was a significant barrier to their translational application in medicine. In the course of our investigations on antimicrobial polymers, we sought to quantify the effect of serum and serum proteins on the activity of polymers in an attempt to find lead candidates that might retain a sufficient degree of their inherent potency in the physiological condition. Copyright: © 2021 by the authors. S. aureus Licensee MDPI, Basel, Switzerland. We are specifically targeting because it is currently one of the most serious This article is an open access article pathogens in the medical field due to the rise in antibiotic drug resistance. The cell wall of distributed under the terms and S. aureus is a tough protective coat, which is relatively amorphous and is 20–40 nm thick [9]. conditions of the Creative Commons Teichoic acids, a major part of a cell wall, contribute together with peptidoglycan to a Attribution (CC BY) license (https:// net negative charge of the staphylococcal cell surface [10]. This Gram-positive, spherical creativecommons.org/licenses/by/ bacterium causes a variety of localized and more invasive infections, especially when the 4.0/). skin or a mucosal barrier is breached [11]. S. aureus colonizes and infects both hospitalized Molecules 2021, 26, 4512. https://doi.org/10.3390/molecules26154512 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 8 Molecules 2021, 26, 4512 net negative charge of the staphylococcal cell surface [10]. This Gram-positive, spherical2 of 8 bacterium causes a variety of localized and more invasive infections, especially when the skin or a mucosal barrier is breached [11]. S. aureus colonizes and infects both hospitalized patients with decreased immunity and healthy immunocompetent patients [10]. Thus, patients with decreased immunity and healthy immunocompetent patients [10]. Thus, there remains an urgent and unmet need for new antimicrobials effective in eradicating there remains an urgent and unmet need for new antimicrobials effective in eradicating S. S. aureus infection. Surprisingly, we discovered that the activity of cationic homopolymers aureus infection. Surprisingly, we discovered that the activity of cationic homopolymers of of aminoethyl methacrylate against S. aureus is in fact enhanced in the presence of fetal aminoethyl methacrylate against S. aureus is in fact enhanced in the presence of fetal bovine bovine serum (FBS), an intriguing result that stands in stark contrast with conventional serum (FBS), an intriguing result that stands in stark contrast with conventional wisdom wisdom in the field. Here, we extended our investigation to cationic amphiphilic copoly- in the field. Here, we extended our investigation to cationic amphiphilic copolymers mers with hydrophobic side chains, which mimic the properties of AMPs, and propose a with hydrophobic side chains, which mimic the properties of AMPs, and propose a new new hypothesis to explain this potentially valuable phenomenon. hypothesis to explain this potentially valuable phenomenon. 2. Results and Discussion In this study, wewe reportreport our our discovery discovery that that serum serum potentiates potentiates the the antimicrobial antimicrobial activity activ- ofity AMP-mimeticof AMP-mimetic methacrylate methacrylate copolymers copolymers against againstS. aureusS. aureus. Despite. Despite the the ever-increasing ever-increas- abundanceing abundance of literature of literature on antimicrobialon antimicrobial polymers, polymers, we we could could find find no no report report quantifying quantify- theing effectsthe effects of whole of whole serum serum and and serum serum proteins protei onns antibacterial on antibacterial polymer polymer activity activity (perhaps (per- duehaps to due the to prevailing the prevailing view thatview serum that proteinsserum proteins will inactivate will inactivate these antibacterial these antibacterial agents, underminingagents, undermining their potential their application).potential application). Since the serumSince effectthe serum is rather effect important is rather for im- the nextportant step for into the translational next step into work, translational we therefore work, endeavored we therefore to screen endeavored a library of to prototypical screen a li- antibacterialbrary of prototypical polymethacrylates antibacterial for activity polymethacrylates in the growth for media activity (MH in broth) the growth supplemented media with(MH serum.broth) supplemented with serum. The methacrylate copolymers consist of randomrandom sequencessequences ofof cationiccationic aminoethylaminoethyl methacrylate and and hydrophobic hydrophobic alkyl alkyl (methyl (methyl or orbutyl) butyl) methacrylates methacrylates (as illustrated (as illustrated in Fig- in Figureure 1),1 which), which were were designed designed to mimic to mimic the cationic the cationic amphiphilic amphiphilic structure structure and the and mem- the membrane-disruptingbrane-disrupting function function of AMPs of AMPs[12]. The [12 synthesis]. The synthesis and characterization and characterization were reported were reportedpreviously previously [13]. In this [13]. study, In this we study, focused we focused on a representative on a representative panel panel of low of lowmolecular molec- ularweight weight polymers polymers (2–3 kDa), (2–3 kDa),which which mimic mimic the small the molecular small molecular size of sizeAMPs. of AMPs.The (co)pol- The (co)polymersymers are denoted are denoted as P0, asMPx,0 ,andMx ,B andx. TheBx .letter The letter indicates indicates either either a homopolymer a homopolymer (P0 ()P or0) orcopolymers copolymers with with methyl methyl (M (M) or) or butyl butyl (B (B) )side side chains, chains, whereas whereas xx indicates the averageaverage mole% of methyl or butyl groups in thethe copolymerscopolymers (as(as illustratedillustrated inin TableTable1 1).). O H O H x n MeO S 1-x MeO S n O O O O O O Mx: R = Me R P0 Bx: R = Bu x = mol % R NH3 NH3 Figure 1. Structure of cationic, amphiphilic (co)polymethacrylates. Table 1.1. CharacterizationCharacterization ofof (co)polymers.(co)polymers. a b PolymerPolymer RR %R%R DP DP a MMn nb P0P0 -- 00 14 14 2320 2320 M M1010 MeMe 1010 14 14 2200 2200 M28 Me 28 15 2170 M28 Me 28 15 2170 M47 Me 47 20 2640 47 MM63 MeMe 6347 20 17 2640 2070 BM27 63 BuMe 2763 17 16 2070 2530 a Degree ofB polymerization27 basedBu on NMR end-group27 analysis; b number16 average molecular2530 weight
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