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Novel formulation of antimicrobial peptides enhances antimicrobial activity against methicillin-resistant Staphylococcus aureus (MRSA)

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Abstract

Antimicrobial peptides (AMPs) have the ability to penetrate as well as transport cargo across bacterial cell membranes, and they have been labeled as exceptional candidates to function in drug delivery. The aim of this study was to investigate the effectiveness of novel formulation of AMPs for enhanced MRSA activity. The strategy was carried out through the formulation of liposomes by thin-layer film hydration methodology, containing phosphatidylcholine, cholesterol, oleic acid, the novel AMP, as well as vancomycin (VCM). Characterization of the AMPs and liposomes included HPLC and LCMS for peptide purity and mass determination; DLS (size, polydispersity, zeta potential), TEM (surface morphology), dialysis (drug release), broth dilution, and flow cytometry (antibacterial activity); MTT assay, haemolysis and intracellular antibacterial studies. The size, PDI, and zeta potential of the drug-loaded AMP2-Lipo-1 were 102.6 ± 1.81 nm, 0.157 ± 0.01, and − 9.81 ± 1.69 mV, respectively, while for AMP3-Lipo-2 drug-loaded formulation, it was 146.4 ± 1.90 nm, 0.412 ± 0.05, and − 4.27 ± 1.25 mV respectively at pH 7.4. However, in acidic pH for both formulations, we observed an increase in size, PDI, and a switch to positive zeta potential, which indicated the pH responsiveness of our liposomal systems. The in vitro drug release studies demonstrated that liposomal formulations released VCM-HCl at a faster rate at pH 6.0 compared to pH 7.4. In vitro antibacterial activity against S. aureus and MRSA revealed that liposomes had enhanced activity at pH 6 compared to pH 7.4. The study revealed that the formulation can potentially be used to enhance activity and penetration of AMPs, thereby improving the treatment of bacterial infections.

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References

  • Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2:19–25

    Google Scholar 

  • Abu Lila AS, Ishida T (2017) Liposomal delivery systems: design optimization and current applications. Biol Pharm Bull 40:1–10

    CAS  Google Scholar 

  • Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, Samiei M, Kouhi M, Nejati-Koshki K (2013) Liposome: classification, preparation, and applications. Nanoscale Res Lett 8:102

    Google Scholar 

  • Alves ID, Goasdoué N, Correia I, Aubry S, Galanth C, Sagan S, Lavielle S, Chassaing G (2008) Membrane interaction and perturbation mechanisms induced by two cationic cell penetrating peptides with distinct charge distribution. Biochim Biophys Acta Gen Subj 1780:948–959

    CAS  Google Scholar 

  • Antimicrobial cell penetrating peptides with bacterial cell specificity (2018) Pharmacophore modeling, quantitative structure activity relationship and molecular dynamics simulation. J Biomol Struct Dyn 1:153–173

    Google Scholar 

  • Arias M, Piga KB, Hyndman ME, Vogel HJ (2018) Improving the activity of Trp-rich antimicrobial peptides by Arg/Lys Substitutions and changing the length of cationic residues. Biomolecules 8:19

    Google Scholar 

  • Bahnsen JS, Franzyk H, Sandberg-Schaal A, Nielsen HM (1828) Antimicrobial and cell-penetrating properties of penetratin analogs: Effect of sequence and secondary structure. Biochim Biophys Acta Biomembr 2013:223–232

    Google Scholar 

  • Biswaro LS, Sousa MG, Rezende TMB, Dias SC, Franco OL (2018) Antimicrobial peptides and nanotechnology, recent advances and challenges. Front Microbiol 9:855

    Google Scholar 

  • Bozzuto G, Molinari A (2015) Liposomes as nanomedical devices. Int J Nanomed 10:975

    CAS  Google Scholar 

  • Brauner A, Fridman O, Gefen O, Balaban NQ (2016) Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat Rev Microbiol 14:320

    CAS  Google Scholar 

  • Brinch KS, Tulkens PM, Van Bambeke F, Frimodt-Møller N, Høiby N, Kristensen H-H (2010) Intracellular activity of the peptide antibiotic NZ2114: studies with Staphylococcus aureus and human THP-1 monocytes, and comparison with daptomycin and vancomycin. J Antimicrob Chemother 65:1720–1724

    CAS  Google Scholar 

  • Bulbake U, Doppalapudi S, Kommineni N, Khan W (2017) Liposomal formulations in clinical use: an updated review. Pharmaceutics 9:12

    Google Scholar 

  • Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126:14101

    Google Scholar 

  • Caldeira S, de Araújo Lopes M, Novais VM, Salviano Teixeira C, Honorato-Sampaio K, Tadeu Pereira M, Ferreira LAM, Braga FC, Cristina Oliveira M (2013) Preparation, physicochemical characterization, and cell viability evaluation of long-circulating and pH-sensitive liposomes containing ursolic acid. Biomed Res Int 13:190–345

    Google Scholar 

  • Cao B, Christophersen L, Thomsen K, Sønderholm M, Bjarnsholt T, Jensen PØ, Høiby N, Moser C (2015) Antibiotic penetration and bacterial killing in a Pseudomonas aeruginosa biofilm model. J Antimicrob Chemother 70:2057–2063

    CAS  Google Scholar 

  • Carmona-Ribeiro AM, de Melo Carrasco LD (2014) Novel formulations for antimicrobial peptides. Int J Mol Sci 15:18040–18083

    CAS  Google Scholar 

  • Chambers HF, DeLeo FR (2009) Waves of resistance: Staphylococcus aureus in the Antibiotic Era. Nat Rev Microbiol 7:629–641

    CAS  Google Scholar 

  • Chatin B, Mével M, Devallière J, Dallet L, Haudebourg T, Peuziat P, Colombani T, Berchel M, Lambert O, Edelman A, Pitard B (2015) Liposome-based formulation for intracellular delivery of functional proteins. Mol Ther Nucleic Acids 4:e244

    CAS  Google Scholar 

  • Chiang C-Y, Uzoma I, Moore RT, Gilbert M, Duplantier AJ, Panchal RG (2018) Mitigating the impact of antibacterial drug resistance through host-directed therapies: current progress, outlook, and challenges. Mbio 9:18

    Google Scholar 

  • Close WL, Glassbrook JE, Gurczynski SJ, Pellett PE (2018) Infection-induced changes within the endocytic recycling compartment suggest a roadmap of human cytomegalovirus egress. Front. Microbiol 9:2

    Google Scholar 

  • de Jong DH, Singh G, Bennett WFD, Arnarez C, Wassenaar TA, Schafer LV, Periole X, Tieleman DP, Marrink SJ (2013) Improved parameters for the martini coarse-grained protein force field. J Chem Theory Comput 9:687–697

    Google Scholar 

  • Desai P, Patlolla RR, Singh M (2010) Interaction of nanoparticles and cell-penetrating peptides with skin for transdermal drug delivery. Mol Membr Biol 27:247–259

    CAS  Google Scholar 

  • Deshpande PP, Biswas S, Torchilin VP (2013) Current trends in the use of liposomes for tumor targeting. Nanomedicine 8:1509–1528

    CAS  Google Scholar 

  • Epand RM, Epand RF (2009) Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta Biomembr 1788:289–294

    CAS  Google Scholar 

  • Epand RM, Walker C, Epand RF, Magarvey NA (1858) Molecular mechanisms of membrane targeting antibiotics. Biochim Biophys Acta Biomembr 2016:980–987

    Google Scholar 

  • Exl L, Bance S, Reichel F, Schrefl T, Peter Stimming H, Mauser NJ (2014) LaBonte’s method revisited: an effective steepest descent method for micromagnetic energy minimization. J Appl Phys 115:17D118

    Google Scholar 

  • Gautam A, Chaudhary K, Kumar R, Sharma A, Kapoor P, Tyagi A, Raghava GPS (2013) In silico approaches for designing highly effective cell penetrating peptides. J Transl Med 11:74

    CAS  Google Scholar 

  • Gautam A, Chaudhary K, Kumar R, Raghava GPS (2015) Computer-aided virtual screening and designing of cell-penetrating peptides. Springer, London

    Google Scholar 

  • Grant SS, Hung DT (2013) Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence 4:273–283

    Google Scholar 

  • Han J, Huang Y, Chen X, Zhou F, Fei Y, Fu J (2018) Lipidation and conformational constraining for prolonging the effects of peptides: Xenopus glucagon-like peptide 1 analogues with potent and long-acting hypoglycemic activity. Eur J Pharm Sci 123:111–123

    CAS  Google Scholar 

  • Hansen A, Schäfer I, Knappe D, Seibel P, Hoffmann R (2012) Intracellular toxicity of proline-rich antimicrobial peptides shuttled into mammalian cells by the cell-penetrating peptide penetratin. Antimicrob Agents Chem 56:5194–5201

    CAS  Google Scholar 

  • Heidarli E, Dadashzadeh S, Haeri A (2017) State of the art of stimuli-responsive liposomes for cancer therapy. Iran J Pharm Res IJPR 16:1273–1304

    CAS  Google Scholar 

  • Hendricks MP, Sato K, Palmer LC, Stupp SI (2017) Supramolecular assembly of peptide. Amphiphiles 1:2440–2448

    Google Scholar 

  • Hsu C-Y, Yang S-C, Sung CT, Weng Y-H, Fang J-Y (2017) Anti-MRSA malleable liposomes carrying chloramphenicol for ameliorating hair follicle targeting. Int J Nanomed 12:8227–8238

    CAS  Google Scholar 

  • Hu X, Zhang Y, Xie Z, Jing X, Bellotti A, Gu Z (2017) Stimuli-responsive polymersomes for biomedical applications. Biomacromol 18:649–673

    CAS  Google Scholar 

  • Irazazabal LN, Porto WF, Ribeiro SM, Casale S, Humblot V, Ladram A, Franco OL (1858) Selective amino acid substitution reduces cytotoxicity of the antimicrobial peptide mastoparan. Biochim Biophys Acta Biomembr 2016:2699–2708

    Google Scholar 

  • Jo S, Cheng X, Lee J, Kim S, Park S-J, Patel DS, Beaven AH, Rui KH, Park S, Lee HS, Roux B, MacKerell AD Jr, Klauda JB, Qi Y, Im W (2017) CHARMM-GUI 10 years for biomolecular modeling and simulation. J Comput Chem 38:1114–1124

    CAS  Google Scholar 

  • Jorgensen JH, Turnidge JD (2015) Susceptibility test methods: dilution and disk diffusion methods. Am Soc Microbiol 1:1253–1273

    Google Scholar 

  • Kalhapure RS, Akamanchi KG (2012) Oleic acid based heterolipid synthesis, characterization and application in self-microemulsifying drug delivery system. Int J Pharm 425:9–18

    CAS  Google Scholar 

  • Kalhapure RS, Sikwal DR, Rambharose S, Mocktar C, Singh S, Bester L, Oh JK, Renukuntla J, Govender T (2017) Enhancing targeted antibiotic therapy via pH responsive solid lipid nanoparticles from an acid cleavable lipid, nanomedicine nanotechnology. Biol Med 13:2067–2077

    CAS  Google Scholar 

  • Kamaruzzaman NF, Kendall S, Good L (2017) Targeting the hard to reach: challenges and novel strategies in the treatment of intracellular bacterial infections. Br J Pharmacol 174:2225–2236

    CAS  Google Scholar 

  • Khan HA, Ahmad A, Mehboob R (2015) Nosocomial infections and their control strategies. Asian Pac J Trop Biomed 5:509–514

    Google Scholar 

  • Lamichhane N, Udayakumar TS, D’Souza WD, Simone CB II, Raghavan SR, Polf J, Mahmood J (2018) Liposomes: clinical applications and potential for image-guided drug delivery. Molecules 23:288

    Google Scholar 

  • Lee H, Lim SI, Shin S-H, Lim Y, Koh JW, Yang S (2019) Conjugation of cell-penetrating peptides to antimicrobial peptides enhances antibacterial activity. ACS Omega 4:15694–15701

    CAS  Google Scholar 

  • Leon-Sicairos N, Reyes-Cortes R, Guadrón-Llanos AM, Madueña-Molina J, Leon-Sicairos C, Canizalez-Román A (2015) Strategies of intracellular pathogens for obtaining iron from the environment. Biomed Res Int 5:15

    Google Scholar 

  • Levison ME, Levison JH (2009) Pharmacokinetics and pharmacodynamics of antibacterial agents. Infect Dis Clin 23:791–815

    Google Scholar 

  • Li X-Z, Nikaido H (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69:1555–1623

    CAS  Google Scholar 

  • Li J, Koh J-J, Liu S, Lakshminarayanan R, Verma CS, Beuerman RW (2017) Membrane active antimicrobial peptides: translating mechanistic insights to design. Front Neurosci 11:73

    CAS  Google Scholar 

  • Li J, Xie S, Ahmed S, Wang F, Gu Y, Zhang C, Chai X, Wu Y, Cai J, Cheng G (2017) Antimicrobial activity and resistance: influencing factors. Front Pharmacol 8:364

    Google Scholar 

  • Lin Y, Mao C (2011) Bio-inspired supramolecular self-assembly towards soft nanomaterials. Front Mater Sci 5:247

    Google Scholar 

  • Liu X, Huang G (2013) Formation strategies, mechanism of intracellular delivery and potential clinical applications of pH-sensitive liposomes. Asian J Pharm Sci 8:319–328

    Google Scholar 

  • Liu X, Li Z, Wang X, Chen Y, Wu F, Men K, Xu T, Luo Y, Yang L (2016) Novel antimicrobial peptide–modified azithromycin-loaded liposomes against methicillin-resistant Staphylococcus aureus. Int J Nanomed 11:6781

    CAS  Google Scholar 

  • Lombardo D, Calandra P, Barreca D, Magazù S, Kiselev MA (2016) Soft interaction in liposome nanocarriers for therapeutic drug delivery. Nanomaterials 6:125

    Google Scholar 

  • Malanovic N, Lohner K (2016) Antimicrobial peptides targeting gram-positive bacteria. Pharmaceuticals 9:59

    Google Scholar 

  • Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH (2007) The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B 111:7812–7824

    CAS  Google Scholar 

  • Martens E, Demain AL (2017) The antibiotic resistance crisis, with a focus on the United States. J Antibiot (Tokyo) 70:520

    CAS  Google Scholar 

  • Maya S, Indulekha S, Sukhithasri V, Smitha KT, Nair SV, Jayakumar R, Biswas R (2012) International journal of biological macromolecules efficacy of tetracycline encapsulated O -carboxymethyl chitosan nanoparticles against intracellular infections of Staphylococcus aureus. Int J Biol Macromol 51:392–399

    CAS  Google Scholar 

  • Michael CA, Dominey-Howes D, Labbate M (2014) The antimicrobial resistance crisis: causes, consequences, and management. Front Public Heal 2:145

    Google Scholar 

  • Mishra B, Wang G (2012) Ab initio design of potent anti-MRSA peptides based on database filtering technology. J Am Chem Soc 134:12426–12429

    CAS  Google Scholar 

  • Mishra B, Reiling S, Zarena D, Wang G (2017) Host defense antimicrobial peptides as antibiotics: design and application strategies. Curr Opin Chem Biol 38:87–96

    CAS  Google Scholar 

  • Mishra AK, Choi J, Moon E, Baek K-H (2018) Tryptophan-rich and proline-rich antimicrobial peptides. Molecules 23:815

    Google Scholar 

  • Mohamed MF, Abdelkhalek A, Seleem MN (2016) Evaluation of short synthetic antimicrobial peptides for treatment of drug-resistant and intracellular Staphylococcus aureus. Sci Rep 6:29707

    Google Scholar 

  • Moiset G, Cirac AD, Stuart MCA, Marrink S-J, Sengupta D, Poolman B (2013) Dual action of BPC194: a membrane active peptide killing bacterial cells. PLoS ONE 8:e61541

    CAS  Google Scholar 

  • Nasompag S, Dechsiri P, Hongsing N, Phonimdaeng P, Daduang S, Klaynongsruang S, Camesano TA, Patramanon R (1848) Effect of acyl chain length on therapeutic activity and mode of action of the CX-KYR-NH2 antimicrobial lipopeptide. Biochim Biophys Acta Biomembr 2015:2351–2364

    Google Scholar 

  • Nicolas P (2009) Multifunctional host defense peptides: intracellular-targeting antimicrobial peptides. FEBS J 276:6483–6496

    CAS  Google Scholar 

  • Omolo CA, Kalhapure RS, Jadhav M, Rambharose S, Mocktar C, Ndesendo VMK, Govender T (2017) Pegylated oleic acid: A promising amphiphilic polymer for nano-antibiotic delivery. Eur J Pharm Biopharm 112:96–108

    CAS  Google Scholar 

  • Omolo CA, Megrab NA, Kalhapure RS, Agrawal N, Jadhav M, Mocktar C, Rambharose S, Maduray K, Nkambule B, Govender T (2019) Liposomes with pH responsive ‘on and off’ switches for targeted and intracellular delivery of antibiotics. J Liposome Res 10:1–19

    Google Scholar 

  • Paliwal SR, Paliwal R, Vyas SP (2015) A review of mechanistic insight and application of pH-sensitive liposomes in drug delivery. Drug Deliv 22:231–242

    CAS  Google Scholar 

  • Palm C, Netzereab S, Hällbrink M (2006) Quantitatively determined uptake of cell-penetrating peptides in non-mammalian cells with an evaluation of degradation and antimicrobial effects. Peptides 27:1710–1716

    CAS  Google Scholar 

  • Parrinello M, Rahman A (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52:7182–7190

    CAS  Google Scholar 

  • Qi Y, Cheng X, Han W, Jo S, Schulten K, Im W (2014) CHARMM-GUI PACE CG Builder for solution, micelle, and bilayer coarse-grained simulations. J Chem Inf Model 54:1003–1009

    CAS  Google Scholar 

  • Rajchakit U, Sarojini V (2017) Recent developments in antimicrobial peptide conjugated gold nanoparticles. Bioconj Chem 28(11):2673–2686

    CAS  Google Scholar 

  • Reddy PS, John MS, Devi PV, Reddy BSP (2017) Detection of vancomycin susceptibility among clinical isolates of MRSA by using minimum inhibitory concentration method. Int J Res Med Sci 3:1378–1382

    Google Scholar 

  • Roca I, Akova M, Baquero F, Carlet J, Cavaleri M, Coenen S, Cohen J, Findlay D, Gyssens I, Heure OE (2015) The global threat of antimicrobial resistance: science for intervention. New Microbes New Infect 6:22–29

    CAS  Google Scholar 

  • Rollin G, Tan X, Tros F, Dupuis M, Nassif X, Charbit A, Coureuil M (2017) Intracellular survival of Staphylococcus aureus in endothelial cells: a matter of growth or persistence. Front Microbiol 8:1354

    Google Scholar 

  • Sani M-A, Separovic F (2016) How membrane-active peptides get into lipid membranes. Acc Chem Res 49:1130–1138

    CAS  Google Scholar 

  • Schlusselhuber M, Torelli R, Martini C, Leippe M, Cattoir V, Leclercq R, Laugier C, Grötzinger J, Sanguinetti M, Cauchard J (2013) The equine antimicrobial peptide eCATH1 is effective against the facultative intracellular pathogen Rhodococcus equi in mice. Antimicrob. Agents Chemother. 1:02044

    Google Scholar 

  • Scocchi M, Mardirossian M, Runti G, Benincasa M (2015) Non-membrane permeabilizing modes of action of antimicrobial peptides on bacteria. Curr Top Med Chem 16:76–88

    Google Scholar 

  • Shen Y, Maupetit J (2012) PEP-FOLD : an updated de novo structure prediction server for both linear and disulfide bonded cyclic peptides. Nucleic Acids Res 40:288–293

    Google Scholar 

  • Stubbings W, Leow P, Yong GC, Goh F, Körber-Irrgang B, Kresken M, Endermann R, Labischinski H (2011) Spectrum of activity of finafloxacin, a novel, pH-Activated Fluoroquinolone, under standard and acidic conditions. Antimicrob Agents Chemother 55:4394–4397

    CAS  Google Scholar 

  • Tayo LL (2017) Stimuli-responsive nanocarriers for intracellular delivery. Biophys Rev 9:931–940

    CAS  Google Scholar 

  • Tesei G, Vazdar M, Jensen MR, Cragnell C, Mason PE, Heyda J, Skepö M, Jungwirth P, Lund M (2017) Self-association of a highly charged arginine-rich cell-penetrating peptide. Proc Natl Acad Sci U S A 114:11428–11433

    CAS  Google Scholar 

  • Thevenet P, Shen Y, Maupetit J, Guyon F, Derreumaux P, Tuffery P (2012) PEP-FOLD: an updated de novo structure prediction server for both linear and disulfide bonded cyclic peptides. Nucleic Acids Res 40:W288–W293

    CAS  Google Scholar 

  • Turon P, Valle LJ, Alemán C, Puiggalí J (2017) Biodegradable and biocompatible systems based on hydroxyapatite nanoparticles. Appl Sci 7(1):60

    Google Scholar 

  • van Heijenoort J (2007) Lipid intermediates in the biosynthesis of bacterial peptidoglycan. Microbiol Mol Biol Rev 71:620–635

    Google Scholar 

  • Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther 40:277

    Google Scholar 

  • Wang Y, Zhao T, Wei D, Strandberg E, Ulrich AS, Ulmschneider JP (1838) How reliable are molecular dynamics simulations of membrane active antimicrobial peptides? Biochim Biophys Acta - Biomembr 2014:2280–2288

    Google Scholar 

  • Wang S, Zeng X, Yang Q, Qiao S (2016) Antimicrobial peptides as potential alternatives to antibiotics in food animal industry. Int J Mol Sci 17:603

    Google Scholar 

  • Ward BP, Ottaway NL, Perez-Tilve D, Ma D, Gelfanov VM, Tschöp MH, DiMarchi RD (2013) Peptide lipidation stabilizes structure to enhance biological function. Mol Metab 2:468–479

    CAS  Google Scholar 

  • Watkins RR, Bonomo RA (2016) Overview: global and local impact of antibiotic resistance. Infect Dis Clin 30:313–322

    Google Scholar 

  • Wen Y, Collier JH (2015) Supramolecular peptide vaccines: tuning adaptive immunity. Curr Opin Immunol 35:73–79

    CAS  Google Scholar 

  • WHO (2014) Antimicrobial resistance: global report on surveillance. World Health Organ 12:9

    Google Scholar 

  • Young-Speirs M, Drouin D, Cavalcante PA, Barkema HW, Cobo ER (2018) Host defense cathelicidins in cattle: types, production, bioactive functions and potential therapeutic and diagnostic applications. Int J Antimicrob Agents 8:88

    Google Scholar 

  • Yuenyongviwat V, Ingviya N, Pathaburee P, Tangtrakulwanich B (2017) Inhibitory effects of vancomycin and fosfomycin on methicillin-resistant Staphylococcus aureus from antibiotic-impregnated articulating cement spacers. Bone Joint Res 6:132–136

    CAS  Google Scholar 

  • Zhang H (2017) Thin-film hydration followed by extrusion method for liposome preparation. Methods Mol Biol 1522:17–22

    CAS  Google Scholar 

  • Zhang L, Bulaj G (2012) Converting peptides into drug leads by Lipidation. Curr Med Chem 19(11):1602–1618

    CAS  Google Scholar 

  • Zhang Q, Tang J, Ran R, Liu Y, Zhang Z, Gao H, He Q (2016) Development of an anti-microbial peptide-mediated liposomal delivery system: a novel approach towards pH-responsive anti-microbial peptides. Drug Deliv 23:1163–1170

    CAS  Google Scholar 

  • Zhang X, Lin C, Lu A, Lin G, Chen H, Liu Q, Yang Z, Zhang H (2017) Liposomes equipped with cell penetrating peptide BR2 enhances chemotherapeutic effects of cantharidin against hepatocellular carcinoma. Drug Deliv 24:986–998

    CAS  Google Scholar 

  • Zhu WL, Shin SY (2009) Antimicrobial and cytolytic activities and plausible mode of bactericidal action of the cell penetrating peptide penetratin and its lys-linked two-stranded peptide. Chem Biol Drug Des 73:209–215

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the College of Health Sciences (CHS), University of KwaZulu-Natal (UKZN), UKZN Nanotechnology Platform, and the National Research Foundation (NRF) of South Africa [grant number NRF Grant No. 87790].

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  1. Discipline of Pharmaceutical Sciences, College of Health Sciences, University of KwaZulu-Natal, Private Bag, Durban, X54001, South Africa

    Mbuso Faya, Calvin A. Omolo, Nikhi Agrawal, Ruma Maji, Pavan Walvekar, Chunderika Mocktar & Thirumala Govender

  2. School of Laboratory Medicine and Medical Sciences, College of Health Sciences, University of KwaZulu-Natal, Private Bag, Durban, X54001, South Africa

    Bongani Nkambule

  3. Peptide Science Laboratory, School of Chemistry and Physics, University of KwaZulu-Natal, Durban, 4001, South Africa

    Heba A. Hazzah & Fernando Albericio

  4. KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, College of Health Sciences, University of KwaZulu-Natal Durban, Durban, 4041, South Africa

    Heba A. Hazzah & Beatriz G. de la Torre

  5. Department of Pharmaceutics, School of Pharmacy and Health Sciences, United States International University-Africa, P. O. Box 14634-00800, Nairobi, Kenya

    Calvin A. Omolo

  6. Department of Surgery, Division of Emergency Medicine, University of Cape Town, Cape Town, South Africa

    Sanjeev Rambharose

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  1. Mbuso Faya
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Faya, M., Hazzah, H.A., Omolo, C.A. et al. Novel formulation of antimicrobial peptides enhances antimicrobial activity against methicillin-resistant Staphylococcus aureus (MRSA). Amino Acids 52, 1439–1457 (2020). https://doi.org/10.1007/s00726-020-02903-7

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