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REVIEW

Antimicrobial Peptides and Cell-Penetrating Peptides: Non-Antibiotic Membrane-Targeting Strategies Against Bacterial Infections

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Pages 1203-1219 | Received 07 Nov 2022, Accepted 02 Feb 2023, Published online: 28 Feb 2023

References

  • Laxminarayan R, Matsoso P, Pant S, et al. Access to effective antimicrobials: a worldwide challenge. Lancet. 2016;387(10014):168–175.
  • Epand RM, Walker C, Epand RF, Magarvey NA. Molecular mechanisms of membrane targeting antibiotics. Biochim Biophys Acta Biomembr. 2016;1858(5):980–987.
  • Lima PG, Oliveira JTA, Amaral JL, Freitas CDT, Souza PFN. Synthetic antimicrobial peptides: characteristics, design, and potential as alternative molecules to overcome microbial resistance. Life Sci. 2021;278:119647.
  • Ruiz N, Kahne D, Silhavy TJ. Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol. 2006;4(1):57–66.
  • Hadjicharalambous A, Bournakas N, Newman H, Skynner MJ, Beswick P. Antimicrobial and cell-penetrating peptides: understanding penetration for the design of novel conjugate antibiotics. Antibiotics. 2022;11(11):1636.
  • Claro B, González-Freire E, Calvelo M, et al. Membrane targeting antimicrobial cyclic peptide nanotubes – an experimental and computational study. Colloids Surf B Biointerfaces. 2020;196:111349.
  • Pham TN, Loupias P, Dassonville‐Klimpt A, Sonnet P. Drug delivery systems designed to overcome antimicrobial resistance. Med Res Rev. 2019;39(6):2343–2396.
  • Hamoen LW, Wenzel M. Editorial: antimicrobial peptides - interaction with membrane lipids and proteins. Front Cell Dev Biol. 2017;5:4.
  • Bechinger B, Gorr SU. Antimicrobial peptides: mechanisms of action and resistance. J Dent Res. 2016;96(3):254–260.
  • Moravej H, Moravej Z, Yazdanparast M, et al. Antimicrobial peptides: features, action, and their resistance mechanisms in bacteria. Microb Drug Resist. 2018;24(6):747–767.
  • da Cunha NB, Cobacho NB, Viana JFC, et al. The next generation of antimicrobial peptides (AMPs) as molecular therapeutic tools for the treatment of diseases with social and economic impacts. Drug Discov Today. 2017;22(2):234–248.
  • Wang G, Li X, Wang Z. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 2016;44(D1):D1087–D1093.
  • Kurpe SR, Grishin SY, Surin AK, et al. Antimicrobial and amyloidogenic activity of peptides. can antimicrobial peptides be used against SARS-CoV-2? Int J Mol Sci. 2020;21(24):9552.
  • Mabrouk DM. Antimicrobial peptides: features, applications and the potential use against covid-19. Mol Biol Rep. 2022;49(10):10039–10050.
  • Hancock RE. Peptide antibiotics. Lancet. 1997;349(9049):418–422.
  • Bahar A, Ren D. Antimicrobial peptides. Pharmaceuticals. 2013;6(12):1543–1575.
  • Qiu W-X, Zhang M-K, Liu L-H, et al. A self-delivery membrane system for enhanced anti-tumor therapy. Biomaterials. 2018;161:81–94.
  • Dias C, Rauter AP. Membrane-targeting antibiotics: recent developments outside the peptide space. Future Med Chem. 2019;11(3):211–228.
  • Pushpanathan M, Gunasekaran P, Rajendhran J. Antimicrobial peptides: versatile biological properties. Int J Pept. 2013;2013:675391.
  • Vaara M. Agents that increase the permeability of the outer membrane. Microbiol Rev. 1992;56(3):395–411.
  • Anunthawan T, de la Fuente-Núñez C, Hancock RE, Klaynongsruang S. Cationic amphipathic peptides KT2 and RT2 are taken up into bacterial cells and kill planktonic and biofilm bacteria. Biochim Biophys Acta. 2015;1848(6):1352–1358.
  • Schneider T, Sahl H-G. An oldie but a goodie – cell wall biosynthesis as antibiotic target pathway. Int J Med Microbiol. 2010;300(2–3):161–169.
  • Müller A, Wenzel M, Strahl H, et al. Daptomycin inhibits cell envelope synthesis by interfering with fluid membrane microdomains. Proc Natl Acad Sci. 2016;113(45):E7077–E7086.
  • Omardien S, Drijfhout JW, Vaz FM, et al. Bactericidal activity of amphipathic cationic antimicrobial peptides involves altering the membrane fluidity when interacting with the phospholipid bilayer. Biochim Biophys Acta Biomembr. 2018;1860(11):2404–2415.
  • Schäfer A-B, Wenzel M. A how-to guide for mode of action analysis of antimicrobial peptides. Front Cell Infect Microbiol. 2020;10:540898.
  • Scocchi M, Mardirossian M, Runti G, Benincasa M. Non-membrane permeabilizing modes of action of antimicrobial peptides on bacteria. Curr Top Med Chem. 2016;16(1):76–88.
  • Malanovic N, Lohner K. Gram-positive bacterial cell envelopes: the impact on the activity of antimicrobial peptides. Biochim Biophys Acta. 2016;1858(5):936–946.
  • Pfalzgraff A, Brandenburg K, Weindl G. Antimicrobial peptides and their therapeutic potential for bacterial skin infections and wounds. Front Pharmacol. 2018;9:281.
  • Ciumac D, Gong H, Hu X, Lu JR. Membrane targeting cationic antimicrobial peptides. J Colloid Interface Sci. 2019;537:163–185.
  • Teixeira V, Feio MJ, Bastos M. Role of lipids in the interaction of antimicrobial peptides with membranes. Prog Lipid Res. 2012;51(2):149–177.
  • Yeaman MR, Yount NY. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev. 2003;55(1):27–55.
  • Baxter AA, Lay FT, Poon IKH, Kvansakul M, Hulett MD. Tumor cell membrane-targeting cationic antimicrobial peptides: novel insights into mechanisms of action and therapeutic prospects. Cell Mol Life Sci. 2017;74(20):3809–3825.
  • Marr AK, Gooderham WJ, Hancock RE. Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr Opin Pharmacol. 2006;6(5):468–472.
  • Mahlapuu M, Håkansson J, Ringstad L, Björn C. Antimicrobial peptides: an emerging category of therapeutic agents. Front Cell Infect Microbiol. 2016;6:194.
  • Browne K, Chakraborty S, Chen R, et al. A new era of antibiotics: the clinical potential of antimicrobial peptides. Int J Mol Sci. 2020;21(19):7047.
  • Mahlapuu M, Björn C, Ekblom J. Antimicrobial peptides as therapeutic agents: opportunities and challenges. Crit Rev Biotechnol. 2020;40(7):978–992.
  • Zavascki AP, Goldani LZ, Li J, Nation RL. Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J Antimicrob Chemother. 2007;60(6):1206–1215.
  • Sierra JM, Fusté E, Rabanal F, Vinuesa T, Viñas M. An overview of antimicrobial peptides and the latest advances in their development. Expert Opin Biol Ther. 2017;17(6):663–676.
  • Doern CD. When does 2 plus 2 equal 5? A review of antimicrobial synergy testing. J Clin Microbiol. 2014;52(12):4124–4128.
  • Wu X, Li Z, Li X, et al. Synergistic effects of antimicrobial peptide DP7 combined with antibiotics against multidrug-resistant bacteria. Drug Des Devel Ther. 2017;11:939–946.
  • Freitas ED, Bataglioli RA, Oshodi J, Beppu MM. Antimicrobial peptides and their potential application in antiviral coating agents. Colloids Surf B Biointerfaces. 2022;217:112693.
  • Moretta A, Scieuzo C, Petrone AM, et al. Antimicrobial peptides: a new hope in biomedical and pharmaceutical fields. Front Cell Infect Microbiol. 2021;11. doi:10.3389/fcimb.2021.668632
  • Mba IE, Nweze EI. Antimicrobial peptides therapy: an emerging alternative for treating drug-resistant bacteria. Yale J Biol Med. 2022;95(4):445–463.
  • Boparai JK, Sharma PK. Mini review on antimicrobial peptides, sources, mechanism and recent applications. Protein Pept Lett. 2020;27(1):4–16.
  • Fjell CD, Hiss JA, Hancock RE, Schneider G. Designing antimicrobial peptides: form follows function. Nat Rev Drug Discov. 2011;11(1):37–51.
  • Annunziato G, Costantino G. Antimicrobial peptides (AMPs): a patent review (2015–2020). Expert Opin Ther Pat. 2020;30(12):931–947.
  • Kuppusamy R, Willcox M, Black DS, Kumar N. Short cationic peptidomimetic antimicrobials. Antibiotics. 2019;8(2):44.
  • Drayton M, Kizhakkedathu JN, Straus SK. Towards robust delivery of antimicrobial peptides to combat bacterial resistance. Molecules. 2020;25(13):3048.
  • Rounds T, Straus SK. Lipidation of antimicrobial peptides as a design strategy for future alternatives to antibiotics. Int J Mol Sci. 2020;21(24):9692.
  • Chu H-L, Chih Y-H, Peng K-L, et al. Antimicrobial peptides with enhanced salt resistance and antiendotoxin properties. Int J Mol Sci. 2020;21(18):6810.
  • Faya M, Hazzah HA, Omolo CA, et al. Novel formulation of antimicrobial peptides enhances antimicrobial activity against methicillin-resistant Staphylococcus aureus (MRSA). Amino Acids. 2020;52(10):1439–1457.
  • Yamauchi R, Kawano K, Yamaoka Y, et al. Development of antimicrobial peptide-antibiotic conjugates to improve the outer membrane permeability of antibiotics against gram-negative bacteria. ACS Infect Dis. 2022;8(11):2339–2347.
  • Cardoso MH, Orozco RQ, Rezende SB, et al. Computer-aided design of antimicrobial peptides: are we generating effective drug candidates? Front Microbiol. 2019;10:3097.
  • Raucher D, Ryu JS. Cell-penetrating peptides: strategies for anticancer treatment. Trends Mol Med. 2015;21(9):560–570.
  • Ye J, Liu E, Yu Z, et al. CPP-assisted intracellular drug delivery, what is next? Int J Mol Sci. 2016;17(11):1892.
  • Ruseska I, Zimmer A. Internalization mechanisms of cell-penetrating peptides. Beilstein J Nanotechnol. 2020;11:101–123.
  • Del Rio G, Trejo Perez Mario A, Brizuela Carlos A. Antimicrobial peptides with cell-penetrating activity as prophylactic and treatment drugs. Biosci Rep. 2022;42(9):BSR20221789.
  • Grdisa M. The delivery of biologically active (therapeutic) peptides and proteins into cells. Curr Med Chem. 2011;18(9):1373–1379.
  • Milletti F. Cell-penetrating peptides: classes, origin, and current landscape. Drug Discov Today. 2012;17(15–16):850–860.
  • Gautam A, Chaudhary K, Kumar R, et al. In silico approaches for designing highly effective cell penetrating peptides. J Transl Med. 2013;11:74.
  • De Coupade C, Fittipaldi A, Chagnas V, et al. Novel human-derived cell-penetrating peptides for specific subcellular delivery of therapeutic biomolecules. Biochem J. 2005;390(Pt 2):407–418.
  • Kim H, Kitamatsu M, Ohtsuki T. Enhanced intracellular peptide delivery by multivalent cell-penetrating peptide with bioreducible linkage. Bioorg Med Chem Lett. 2018;28(3):378–381.
  • Deshayes S, Konate K, Aldrian G, Heitz F, Divita G. Interactions of amphipathic CPPs with model membranes. Methods Mol Biol. 2011;683:41–56.
  • Vasconcelos L, Pärn K, Langel U. Therapeutic potential of cell-penetrating peptides. Ther Deliv. 2013;4(5):573–591.
  • Gros E, Deshayes S, Morris MC, et al. A non-covalent peptide-based strategy for protein and peptide nucleic acid transduction. Biochim Biophys Acta. 2006;1758(3):384–393.
  • Derakhshankhah H, Jafari S. Cell penetrating peptides: a concise review with emphasis on biomedical applications. Biomed Pharmacother. 2018;108:1090–1096.
  • Böhmová E, Machová D, Pechar M, et al. Cell-penetrating peptides: a useful tool for the delivery of various cargoes into cells. Physiol Res. 2018;67(Suppl 2):S267–S279.
  • Nasrollahi SA, Taghibiglou C, Azizi E, Farboud ES. Cell-penetrating peptides as a novel transdermal drug delivery system. Chem Biol Drug Des. 2012;80(5):639–646.
  • Zorko M, Langel Ü. Studies of cell-penetrating peptides by biophysical methods. Q Rev Biophys. 2022;1–55:e3.
  • Maiolo JR, Ferrer M, Ottinger EA. Effects of cargo molecules on the cellular uptake of arginine-rich cell-penetrating peptides. Biochim Biophys Acta. 2005;1712(2):161–172.
  • Ramsey JD, Flynn NH. Cell-penetrating peptides transport therapeutics into cells. Pharmacol Ther. 2015;154:78–86.
  • Gestin M, Dowaidar M, Langel Ü. Uptake mechanism of cell-penetrating peptides. In: Peptides and Peptide-Based Biomaterials and their Biomedical Applications. Springer;2017:255–264.
  • Kardani K, Milani A, Shabani S, Bolhassani A. Cell penetrating peptides: the potent multi-cargo intracellular carriers. Expert Opin Drug Deliv. 2019;16(11):1227–1258.
  • Ruczynski J, Wierzbicki PM, Kogut-Wierzbicka M, Mucha P, Siedlecka-Kroplewska K, Rekowski P. Cell-penetrating peptides as a promising tool for delivery of various molecules into the cells. Folia Histochem Cytobiol. 2014;52(4):257–269.
  • Wadia JS, Stan RV, Dowdy SF. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med. 2004;10(3):310–315.
  • Thorén PE, Persson D, Isakson P, Goksör M, Onfelt A, Nordén B. Uptake of analogs of penetratin, Tat(48–60) and oligoarginine in live cells. Biochem Biophys Res Commun. 2003;307(1):100–107.
  • Derossi D, Chassaing G, Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 1998;8(2):84–87.
  • Guidotti G, Brambilla L, Rossi D. Cell-penetrating peptides: from basic research to clinics. Trends Pharmacol Sci. 2017;38(4):406–424.
  • Futaki S, Nakase I, Tadokoro A, Takeuchi T, Jones AT. Arginine-rich peptides and their internalization mechanisms. Biochem Soc Trans. 2007;35(Pt 4):784–787.
  • Nam SH, Park J, Koo H. Recent advances in selective and targeted drug/gene delivery systems using cell-penetrating peptides. Arch Pharm Res. 2023;46:18–34.
  • Bechara C, Sagan S. Cell‐penetrating peptides: 20 years later, where do we stand? FEBS Lett. 2013;587(12):1693–1702.
  • Szabó I, Yousef M, Soltész D, Bató C, Mező G, Bánóczi Z. Redesigning of cell-penetrating peptides to improve their efficacy as a drug delivery system. Pharmaceutics. 2022;14(5):907.
  • Ter-Avetisyan G, Tünnemann G, Nowak D, et al. Cell entry of arginine-rich peptides is independent of endocytosis. J Biol Chem. 2009;284(6):3370–3378.
  • Hillaireau H, Couvreur P. Nanocarriers’ entry into the cell: relevance to drug delivery. Cell Mol Life Sci. 2009;66(17):2873–2896.
  • Yang J, Luo Y, Shibu MA, Toth I, Skwarczynskia M. Cell-penetrating peptides: efficient vectors for vaccine delivery. Curr Drug Deliv. 2019;16(5):430–443.
  • Maeng J, Lee K. Systemic and brain delivery of antidiabetic peptides through nasal administration using cell-penetrating peptides. Front Pharmacol. 2022;13:1068495.
  • Habault J, Poyet J-L. Recent advances in cell penetrating peptide-based anticancer therapies. Molecules. 2019;24(5):927.
  • Bolhassani A, Jafarzade BS, Mardani G. In vitro and in vivo delivery of therapeutic proteins using cell penetrating peptides. Peptides. 2017;87:50–63.
  • Zahid M, Robbins P. Cell-type specific penetrating peptides: therapeutic promises and challenges. Molecules. 2015;20(7):13055–13070.
  • Feni L, Neundorf I. The current role of cell-penetrating peptides in cancer therapy. In: Peptides and Peptide-Based Biomaterials and Their Biomedical Applications. Springer;2017:279–295.
  • Lundberg P, El-Andaloussi S, Sütlü T, Johansson H, Langel U. Delivery of short interfering RNA using endosomolytic cell-penetrating peptides. FASEB J. 2007;21(11):2664–2671.
  • Reissmann S. Cell penetration: scope and limitations by the application of cell-penetrating peptides. J Pept Sci. 2014;20(10):760–784.
  • Skotland T, Iversen T, Torgersen M, Sandvig K. Cell-penetrating peptides: possibilities and challenges for drug delivery in vitro and in vivo. Molecules. 2015;20(7):13313–13323.
  • Park SE, Sajid MI, Parang K, Tiwari RK. Cyclic cell-penetrating peptides as efficient intracellular drug delivery tools. Mol Pharm. 2019;16(9):3727–3743.
  • Kozhikhova KV, Andreev SM, Shilovskiy IP, et al. A novel peptide dendrimer LTP efficiently facilitates transfection of mammalian cells. Org Biomol Chem. 2018;16(43):8181–8190.
  • Tesei G, Vazdar M, Jensen MR, et al. Self-association of a highly charged arginine-rich cell-penetrating peptide. Proc Natl Acad Sci U S A. 2017;114(43):11428–11433.
  • Demizu Y, Oba M, Okitsu K, et al. A preorganized β-amino acid bearing a guanidinium side chain and its use in cell-penetrating peptides. Org Biomol Chem. 2015;13(20):5617–5620.
  • Copolovici DM, Langel K, Eriste E, Langel Ü. Cell-penetrating peptides: design, synthesis, and applications. ACS nano. 2014;8(3):1972–1994.
  • Ezzat K, Andaloussi SE, Zaghloul EM, et al. PepFect 14, a novel cell-penetrating peptide for oligonucleotide delivery in solution and as solid formulation. Nucleic Acids Res. 2011;39(12):5284–5298.
  • Kang Z, Ding G, Meng Z, Meng Q. The rational design of cell-penetrating peptides for application in delivery systems. Peptides. 2019;121:170149.
  • Andaloussi SE, Lehto T, Mäger I, et al. Design of a peptide-based vector, PepFect6, for efficient delivery of siRNA in cell culture and systemically in vivo. Nucleic Acids Res. 2011;39(9):3972–3987.
  • El-Sayed A, Futaki S, Harashima H. Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment. AAPS J. 2009;11(1):13–22.
  • Endoh T, Ohtsuki T. Cellular siRNA delivery using cell-penetrating peptides modified for endosomal escape. Adv Drug Deliv Rev. 2009;61(9):704–709.
  • Zhang W, Taheri-Ledari R, Hajizadeh Z, et al. Enhanced activity of vancomycin by encapsulation in hybrid magnetic nanoparticles conjugated to a cell-penetrating peptide. Nanoscale. 2020;12(6):3855–3870.
  • Taheri-Ledari R, Ahghari MR, Ansari F, et al. Synergies in antimicrobial treatment by a levofloxacin-loaded halloysite and gold nanoparticles with a conjugation to a cell-penetrating peptide. Nanoscale Adv. 2022;4(20):4418–4433.
  • Huang Y, Jiang Y, Wang H, et al. Curb challenges of the “Trojan Horse” approach: smart strategies in achieving effective yet safe cell-penetrating peptide-based drug delivery. Adv Drug Deliv Rev. 2013;65(10):1299–1315.
  • Tang B, Zaro JL, Shen Y, et al. Acid-sensitive hybrid polymeric micelles containing a reversibly activatable cell-penetrating peptide for tumor-specific cytoplasm targeting. J Control Release. 2018;279:147–156.
  • Pescina S, Ostacolo C, Gomez-Monterrey IM, et al. Cell penetrating peptides in ocular drug delivery: state of the art. J Control Release. 2018;284:84–102.
  • Luong HX, Thanh TT, Tran TH. Antimicrobial peptides - advances in development of therapeutic applications. Life Sci. 2020;260:118407.
  • Bhattacharjya S, Straus SK. Design, engineering and discovery of novel α-helical and β-boomerang antimicrobial peptides against drug resistant bacteria. Int J Mol Sci. 2020;21(16):5773.
  • Splith K, Neundorf I. Antimicrobial peptides with cell-penetrating peptide properties and vice versa. Eur Biophys J. 2011;40(4):387–397.
  • Pirtskhalava M, Amstrong AA, Grigolava M, et al. DBAASP v3: database of antimicrobial/cytotoxic activity and structure of peptides as a resource for development of new therapeutics. Nucleic Acids Res. 2021;49(D1):D288–D297.
  • Riahifard N, Mozaffari S, Aldakhil T, et al. Design, synthesis, and evaluation of amphiphilic cyclic and linear peptides composed of hydrophobic and positively-charged amino acids as antibacterial agents. Molecules. 2018;23:10.
  • Huan Y, Kong Q, Mou H, Yi H. Antimicrobial peptides: classification, design, application and research progress in multiple fields. Front Microbiol. 2020;11:582779.