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Research article

Environmental Microbiology and Biotechnology (EMB)  |  Protein Engineering and Evolution

Evaluating the Antimicrobial Efficacy of a Designed Synthetic Peptide against Pathogenic Bacteria

Maria Caroline de Moura Cavalheiro1, Caio Fernando Ramalho de Oliveira1, Ana Paula de Araújo Boleti1, Layza Sá Rocha1, Ana Cristina Jacobowski1, Cibele Nicolaski Pedron2, Vani Xavier de Oliveira Júnior2, and Maria Lígia Rodrigues Macedo1*

1Protein Purification Laboratory and its Biological Functions; Faculty of Pharmaceutical Sciences, Food and Nutrition; Faculty of Pharmacy, Food and Nutrition; Federal University of Mato Grosso do Sul (UFMS), Campo Grande, Mato Grosso do Sul, Brazil
2Center for Natural and Human Sciences of the Federal University of ABC (UFABC), São Paulo, SP, Brazil

Correspondence to:
Maria Lígia Rodrigues Macedo,        Ligiamacedo18@gmail.com
Received: May 10, 2024; Revised: August 22, 2024; Accepted: August 26, 2024

J. Microbiol. Biotechnol. 2024; 34(11): 2231-2244

Published November 28, 2024 https://doi.org/10.4014/jmb.2405.05011

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Recent research has focused on discovering peptides that effectively target multidrug-resistant bacteria while leaving healthy cells unharmed. In this work, we describe the antimicrobial properties of RK8, a peptide composed of eight amino acid residues. Its activity was tested against multidrug-resistant Gram-negative and Gram-positive bacteria. RK8's efficacy in eradicating mature biofilm and increasing membrane permeability was assessed using Sytox Green. Cytotoxicity assays were conducted both in vitro and in vivo models. Circular dichroism analysis revealed that RK8 adopted an extended structure in water and sodium dodecyl sulfate (SDS). RK8 exhibited MICs of 8-64 μM and MBCs of 4-64 μM against various bacteria, with higher effectiveness observed in Methicillin-resistant Staphylococcus aureus (MRSA) and E. coli KPC+ strains than others. Ciprofloxacin and Vancomycin showed varying MIC and MBC values lower than RK8 for Gram-positive bacteria, but competitive for Gram-negative bacteria. The combination of RK8 and ciprofloxacin showed a synergistic effect. The RK8 peptides could reduce 38% of the mature Acinetobacter baumannii biofilm. Sytox Green reagent achieved 100% membrane permeation of Gram-positive and Gram-negative bacteria. The RK8 peptide did not show cytotoxic effects against murine macrophages (64 μM), erythrocytes (100 μM) or Galleria mellanella larvae (960 μM). In the stability test against peptidases, the RK8 peptide was stable, maintaining around 60% of the molecule intact after 120 min of incubation. These results highlight the potential of RK8 to be a promising strategy for developing a new antimicrobial and antibiofilm agent, inspiring and motivating further research in antimicrobial peptides.

Keywords

Bacterial resistance, biofilm, drug design

Graphical Abstract


References

  1. Muteeb G, Rehman MT, Shahwan M, Aatif M. 2023. Origin of antibiotics and antibiotic resistance, and their impacts on drug development: A narrative review. Pharmaceuticals 16: 1-54.
    Pubmed PMC
  2. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et al. 2018. Antibiotic resistance: a rundown of a global crisis. Infect. Drug Resist. 11:1645-1658.
    Pubmed PMC
  3. Chinemerem Nwobodo D, Ugwu MC, Oliseloke Anie C, Al-Ouqaili MTS, Chinedu Ikem J, Victor Chigozie U, et al. 2022. Antibiotic resistance: the challenges and emerging strategies for tackling a global menace. J. Clin. Lab. Anal. 36: e24655.
    Pubmed PMC
  4. Terreni M, Taccani M, Pregnolato M. 2021. New antibiotics for multidrug-resistant bacterial strains: latest research developments and future perspectives. Molecules 26: 2671.
    Pubmed PMC
  5. Zhang QY, Yan Z Bin, Meng YM, Hong XY, Shao G, Ma JJ, et al. 2021. Antimicrobial peptides: mechanism of action, activity and clinical potential. Mil. Med. Res. 8: 1-25.
    Pubmed PMC
  6. Lade H, Kim JS. 2021. Bacterial targets of antibiotics in methicillin-resistant Staphylococcus aureus. Antibiotics 10: 398.
    Pubmed PMC
  7. Elibe Mba I, Innocent Nweze E. 2022. Antimicrobial peptides therapy: an emerging alternative for treating drug-resistant bacteria. Yale J. Biol. Med. 95: 445-463.
  8. Pirtskhalava M, Vishnepolsky B, Grigolava M, Managadze G. 2021. Physicochemical features and peculiarities of interaction of amp with the membrane. Pharmaceuticals 14: 471.
    Pubmed PMC
  9. Bakare OO, Gokul A, Niekerk LA, Aina O, Abiona A, Barker AM, et al. 2023. Recent progress in the characterization, Synthesis, delivery procedures, treatment strategies, and precision of antimicrobial peptides. Int. J. Mol. Sci. 24: 11864 .
    Pubmed PMC
  10. Almeida CV, de Oliveira CFR, Almeida LH de O, Ramalho SR, Gutierrez C de O, Sardi J de CO, et al. 2024. Computer-made peptide RQ18 acts as a dual antifungal and antibiofilm peptide though membrane-associated mechanisms of action. Arch. Biochem. Biophys. 753: 109884.
    Pubmed
  11. Wang G, Li X, Wang Z. 2016. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 44(D1): D1087-1093.
    Pubmed PMC
  12. Timmons PB, Hewage CM. 2021. APPTEST is a novel protocol for the automatic prediction of peptide tertiary structures. Brief Bioinform. 22: bbab308.
    Pubmed PMC
  13. BLISS CI. 1939. The toxicity of poisons applied jointly. Ann. Appl. Biol. 26: 585-615.
  14. Almeida CV, de Oliveira CFR, dos Santos EL, dos Santos HF, Júnior EC, Marchetto R, et al. 2021. Differential interactions of the antimicrobial peptide, RQ18, with phospholipids and cholesterol modulate its selectivity for microorganism membranes. Biochim. Biophys. Acta Gen. Subj. 1865: 129937.
    Pubmed
  15. Mohanram H, Bhattacharjya S. 2016. Salt-resistant short antimicrobial peptides. Biopolymers 106: 345-356.
    Pubmed
  16. Walker JN, Horswill AR. 2012. A coverslip-based technique for evaluating Staphylococcus aureus biofilm formation on human plasma. Front. Cell. Infect. Microbiol. 2: 39.
    PMC
  17. Uggerhøj LE, Poulsen TJ, Munk JK, Fredborg M, Sondergaard TE, Frimodt-Moller N, et al. 2015. Rational design of alpha-helical antimicrobial peptides: Do's and don'ts. ChemBioChem. 16: 242-253.
    Pubmed
  18. Mosmann T. 1983 Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
    Pubmed
  19. Powell M, Stewart S, Otvos L, Urge L, Gaeta FCA, Sette A. 1993. Peptide stability in drug development. II. Effect of single amino acid substitution and glycosylation on peptide reactivity in human serum. Pharm. Res. 10: 1268-1273.
    Pubmed
  20. Almaaytah A, Qaoud MT, Mohammed GK, Abualhaijaa A, Knappe D, Hoffmann R, et al. 2018. Antimicrobial and antibiofilm activity of UP-5, an ultrashort antimicrobial peptide designed using only arginine and biphenylalanine. Pharmaceuticals 11: 3.
    Pubmed PMC
  21. Kraszewska J, Beckett MC, James TC, Bond U. 2016. Comparative analysis of the antimicrobial activities of plant defensin-like and ultrashort peptides against food-spoiling bacteria. Appl. Environ. Microbiol. 82: 4288-4298.
    Pubmed PMC
  22. Kalafatovic D, Giralt E. 2017. Cell-penetrating peptides: design strategies beyond primary structure and amphipathicity. Molecules 22: 1929.
    Pubmed PMC
  23. Kardani K, Bolhassani A. 2021. Exploring novel and potent cell penetrating peptides in the proteome of SARS-COV-2 using bioinformatics approaches. PLoS One 16: e0247396.
    Pubmed PMC
  24. Ye H. 2018. Molecular design of antimicrobial peptides based on hemagglutinin fusion domain to combat antibiotic resistance in bacterial infection. J. Pept. Sci. 24. doi: 10.1002/psc.3068.
    Pubmed
  25. WC W. 2010. Describing the mechanism of antimicrobial peptide action with the interfacial activity model. Acs Chem. Biol. 5: 905917.
    Pubmed PMC
  26. Nguyen LT, Haney EF, Vogel HJ. 2011. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 29: 464-472.
    Pubmed
  27. Wei SY, Wu JM, Kuo YY, Chen HL, Yip BS, Tzeng SR, et al. 2006. Solution structure of a novel tryptophan-rich peptide with bidirectional antimicrobial activity. J. Bacteriol. 188: 328-334.
    Pubmed PMC
  28. Almeida LH de O, Oliveira CFR de, Rodrigues M de S, Neto SM, Boleti AP de A, Taveira GB, et al. 2020. Adepamycin: design, synthesis and biological properties of a new peptide with antimicrobial properties. Arch. Biochem. Biophys. 691: 108487.
    Pubmed
  29. McKenna M. 2013. Antibiotic resistance: the last resort. Nature 499: 394-396.
    Pubmed
  30. Menousek J, Mishra B, Hanke ML, Heim CE, Kielian T, Wang G. 2012. Database screening and in vivo efficacy of antimicrobial peptides against methicillin-resistant Staphylococcus aureus USA300. Int. J. Antimicrob. Agents 39: 402-406.
    Pubmed PMC
  31. Das T, Nath C, Das P, Ghosh K, Logno TA, Debnath P, et al. 2023. High prevalence of ciprofloxacin resistance in Escherichia coli isolated from chickens, humans and the environment: an emerging one health issue. PLoS One 18: e0294043.
    Pubmed PMC
  32. Shariati A, Arshadi M, Khosrojerdi MA, Abedinzadeh M, Ganjalishahi M, Maleki A, et al. 2022. The resistance mechanisms of bacteria against ciprofloxacin and new approaches for enhancing the efficacy of this antibiotic. Front. Public Health 10: 1025633.
    Pubmed PMC
  33. Pletzer D, Mansour SC, Hancock REW. 2018. ynergy between conventional antibiotics and anti-biofilm peptides in a murine, subcutaneous abscess model caused by recalcitrant ESKAPE pathogens. PLoS Pathog. 14: e1007084.
    Pubmed PMC
  34. Lin MF, Lin YY, Lan CY. 2019. A method to assess influence of different medical tubing on biofilm formation by Acinetobacter baumannii. J. Microbiol. Methods 160: 84-86.
    Pubmed
  35. Lin Y, Chang RYK, Britton WJ, Morales S, Kutter E, Chan HK. 2018. Synergy of nebulized phage PEV20 and ciprofloxacin combination against Pseudomonas aeruginosa. Int. J. Pharm. 551: 158-165.
    Pubmed PMC
  36. Rishi P, Vashist T, Sharma A, Kaur A, Kaur A, Kaur N, et al. 2018. Efficacy of designer K11 antimicrobial peptide (a hybrid of melittin, cecropin A1 and magainin 2) against Acinetobacter baumannii-infected wounds. Pathog. Dis. 76. doi: 10.1093/femspd/fty072.
    Pubmed
  37. Powers JPS, Hancock REW. 2003. The relationship between peptide structure and antibacterial activity. Peptides 24: 1681-1691.
    Pubmed
  38. Sharma P, Ayappa KG. A 2022. Molecular dynamics study of antimicrobial peptide interactions with the lipopolysaccharides of the outer bacterial membrane. J. Membr. Biol. 255: 665-675.
    Pubmed
  39. Thakur S, Cattoni DI, Nöllmann M. 2015. The fluorescence properties and binding mechanism of SYTOX green, a bright, low photo-damage DNA intercalating agent. Eur. Biophys. J. 44: 337-348.
    Pubmed
  40. Shagaghi N, Palombo EA, Clayton AHA, Bhave M. 2018. Antimicrobial peptides: biochemical determinants of activity and biophysical techniques of elucidating their functionality. World J. Microbiol. Biotechnol. 34: 62.
    Pubmed
  41. Travkova OG, Moehwald H, Brezesinski G. 2017. The interaction of antimicrobial peptides with membranes. Adv. Colloid Interface Sci. 247: 521-532.
    Pubmed
  42. Allegra E, Titball RW, Carter J, Champion OL. 2018. Galleria mellonella larvae allow the discrimination of toxic and non-toxic chemicals. Chemosphere 198: 469-472.
    Pubmed
  43. Browne N, Heelan M, Kavanagh K. 2013. An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 4: 597-603.
    Pubmed PMC
  44. Wojda I. 2017. Immunity of the greater wax moth Galleria mellonella. Insect Sci. 24: 342-357.
    Pubmed
  45. Nguyen LT, Chau JK, Perry NA, de Boer L, Zaat SAJ, Vogel HJ. 2010. Serum stabilities of short tryptophan- and arginine-rich antimicrobial peptide analogs. PLoS One 5: e12684.
    Pubmed PMC
  46. Jia F, Zhang Y, Wang J, Peng J, Zhao P, Zhang L, et al. 2019. The effect of halogenation on the antimicrobial activity, antibiofilm activity, cytotoxicity and proteolytic stability of the antimicrobial peptide Jelleine-I. Peptides 112: 56-66.
    Pubmed

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Article

Research article

J. Microbiol. Biotechnol. 2024; 34(11): 2231-2244

Published online November 28, 2024 https://doi.org/10.4014/jmb.2405.05011

Copyright © The Korean Society for Microbiology and Biotechnology.

Evaluating the Antimicrobial Efficacy of a Designed Synthetic Peptide against Pathogenic Bacteria

Maria Caroline de Moura Cavalheiro1, Caio Fernando Ramalho de Oliveira1, Ana Paula de Araújo Boleti1, Layza Sá Rocha1, Ana Cristina Jacobowski1, Cibele Nicolaski Pedron2, Vani Xavier de Oliveira Júnior2, and Maria Lígia Rodrigues Macedo1*

1Protein Purification Laboratory and its Biological Functions; Faculty of Pharmaceutical Sciences, Food and Nutrition; Faculty of Pharmacy, Food and Nutrition; Federal University of Mato Grosso do Sul (UFMS), Campo Grande, Mato Grosso do Sul, Brazil
2Center for Natural and Human Sciences of the Federal University of ABC (UFABC), São Paulo, SP, Brazil

Correspondence to:Maria Lígia Rodrigues Macedo,        Ligiamacedo18@gmail.com

Received: May 10, 2024; Revised: August 22, 2024; Accepted: August 26, 2024

Abstract

Recent research has focused on discovering peptides that effectively target multidrug-resistant bacteria while leaving healthy cells unharmed. In this work, we describe the antimicrobial properties of RK8, a peptide composed of eight amino acid residues. Its activity was tested against multidrug-resistant Gram-negative and Gram-positive bacteria. RK8's efficacy in eradicating mature biofilm and increasing membrane permeability was assessed using Sytox Green. Cytotoxicity assays were conducted both in vitro and in vivo models. Circular dichroism analysis revealed that RK8 adopted an extended structure in water and sodium dodecyl sulfate (SDS). RK8 exhibited MICs of 8-64 μM and MBCs of 4-64 μM against various bacteria, with higher effectiveness observed in Methicillin-resistant Staphylococcus aureus (MRSA) and E. coli KPC+ strains than others. Ciprofloxacin and Vancomycin showed varying MIC and MBC values lower than RK8 for Gram-positive bacteria, but competitive for Gram-negative bacteria. The combination of RK8 and ciprofloxacin showed a synergistic effect. The RK8 peptides could reduce 38% of the mature Acinetobacter baumannii biofilm. Sytox Green reagent achieved 100% membrane permeation of Gram-positive and Gram-negative bacteria. The RK8 peptide did not show cytotoxic effects against murine macrophages (64 μM), erythrocytes (100 μM) or Galleria mellanella larvae (960 μM). In the stability test against peptidases, the RK8 peptide was stable, maintaining around 60% of the molecule intact after 120 min of incubation. These results highlight the potential of RK8 to be a promising strategy for developing a new antimicrobial and antibiofilm agent, inspiring and motivating further research in antimicrobial peptides.

Keywords: Bacterial resistance, biofilm, drug design

References

  1. Muteeb G, Rehman MT, Shahwan M, Aatif M. 2023. Origin of antibiotics and antibiotic resistance, and their impacts on drug development: A narrative review. Pharmaceuticals 16: 1-54.
    Pubmed KoreaMed
  2. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et al. 2018. Antibiotic resistance: a rundown of a global crisis. Infect. Drug Resist. 11:1645-1658.
    Pubmed KoreaMed
  3. Chinemerem Nwobodo D, Ugwu MC, Oliseloke Anie C, Al-Ouqaili MTS, Chinedu Ikem J, Victor Chigozie U, et al. 2022. Antibiotic resistance: the challenges and emerging strategies for tackling a global menace. J. Clin. Lab. Anal. 36: e24655.
    Pubmed KoreaMed
  4. Terreni M, Taccani M, Pregnolato M. 2021. New antibiotics for multidrug-resistant bacterial strains: latest research developments and future perspectives. Molecules 26: 2671.
    Pubmed KoreaMed
  5. Zhang QY, Yan Z Bin, Meng YM, Hong XY, Shao G, Ma JJ, et al. 2021. Antimicrobial peptides: mechanism of action, activity and clinical potential. Mil. Med. Res. 8: 1-25.
    Pubmed KoreaMed
  6. Lade H, Kim JS. 2021. Bacterial targets of antibiotics in methicillin-resistant Staphylococcus aureus. Antibiotics 10: 398.
    Pubmed KoreaMed
  7. Elibe Mba I, Innocent Nweze E. 2022. Antimicrobial peptides therapy: an emerging alternative for treating drug-resistant bacteria. Yale J. Biol. Med. 95: 445-463.
  8. Pirtskhalava M, Vishnepolsky B, Grigolava M, Managadze G. 2021. Physicochemical features and peculiarities of interaction of amp with the membrane. Pharmaceuticals 14: 471.
    Pubmed KoreaMed
  9. Bakare OO, Gokul A, Niekerk LA, Aina O, Abiona A, Barker AM, et al. 2023. Recent progress in the characterization, Synthesis, delivery procedures, treatment strategies, and precision of antimicrobial peptides. Int. J. Mol. Sci. 24: 11864 .
    Pubmed KoreaMed
  10. Almeida CV, de Oliveira CFR, Almeida LH de O, Ramalho SR, Gutierrez C de O, Sardi J de CO, et al. 2024. Computer-made peptide RQ18 acts as a dual antifungal and antibiofilm peptide though membrane-associated mechanisms of action. Arch. Biochem. Biophys. 753: 109884.
    Pubmed
  11. Wang G, Li X, Wang Z. 2016. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 44(D1): D1087-1093.
    Pubmed KoreaMed
  12. Timmons PB, Hewage CM. 2021. APPTEST is a novel protocol for the automatic prediction of peptide tertiary structures. Brief Bioinform. 22: bbab308.
    Pubmed KoreaMed
  13. BLISS CI. 1939. The toxicity of poisons applied jointly. Ann. Appl. Biol. 26: 585-615.
  14. Almeida CV, de Oliveira CFR, dos Santos EL, dos Santos HF, Júnior EC, Marchetto R, et al. 2021. Differential interactions of the antimicrobial peptide, RQ18, with phospholipids and cholesterol modulate its selectivity for microorganism membranes. Biochim. Biophys. Acta Gen. Subj. 1865: 129937.
    Pubmed
  15. Mohanram H, Bhattacharjya S. 2016. Salt-resistant short antimicrobial peptides. Biopolymers 106: 345-356.
    Pubmed
  16. Walker JN, Horswill AR. 2012. A coverslip-based technique for evaluating Staphylococcus aureus biofilm formation on human plasma. Front. Cell. Infect. Microbiol. 2: 39.
    KoreaMed
  17. Uggerhøj LE, Poulsen TJ, Munk JK, Fredborg M, Sondergaard TE, Frimodt-Moller N, et al. 2015. Rational design of alpha-helical antimicrobial peptides: Do's and don'ts. ChemBioChem. 16: 242-253.
    Pubmed
  18. Mosmann T. 1983 Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
    Pubmed
  19. Powell M, Stewart S, Otvos L, Urge L, Gaeta FCA, Sette A. 1993. Peptide stability in drug development. II. Effect of single amino acid substitution and glycosylation on peptide reactivity in human serum. Pharm. Res. 10: 1268-1273.
    Pubmed
  20. Almaaytah A, Qaoud MT, Mohammed GK, Abualhaijaa A, Knappe D, Hoffmann R, et al. 2018. Antimicrobial and antibiofilm activity of UP-5, an ultrashort antimicrobial peptide designed using only arginine and biphenylalanine. Pharmaceuticals 11: 3.
    Pubmed KoreaMed
  21. Kraszewska J, Beckett MC, James TC, Bond U. 2016. Comparative analysis of the antimicrobial activities of plant defensin-like and ultrashort peptides against food-spoiling bacteria. Appl. Environ. Microbiol. 82: 4288-4298.
    Pubmed KoreaMed
  22. Kalafatovic D, Giralt E. 2017. Cell-penetrating peptides: design strategies beyond primary structure and amphipathicity. Molecules 22: 1929.
    Pubmed KoreaMed
  23. Kardani K, Bolhassani A. 2021. Exploring novel and potent cell penetrating peptides in the proteome of SARS-COV-2 using bioinformatics approaches. PLoS One 16: e0247396.
    Pubmed KoreaMed
  24. Ye H. 2018. Molecular design of antimicrobial peptides based on hemagglutinin fusion domain to combat antibiotic resistance in bacterial infection. J. Pept. Sci. 24. doi: 10.1002/psc.3068.
    Pubmed
  25. WC W. 2010. Describing the mechanism of antimicrobial peptide action with the interfacial activity model. Acs Chem. Biol. 5: 905917.
    Pubmed KoreaMed
  26. Nguyen LT, Haney EF, Vogel HJ. 2011. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 29: 464-472.
    Pubmed
  27. Wei SY, Wu JM, Kuo YY, Chen HL, Yip BS, Tzeng SR, et al. 2006. Solution structure of a novel tryptophan-rich peptide with bidirectional antimicrobial activity. J. Bacteriol. 188: 328-334.
    Pubmed KoreaMed
  28. Almeida LH de O, Oliveira CFR de, Rodrigues M de S, Neto SM, Boleti AP de A, Taveira GB, et al. 2020. Adepamycin: design, synthesis and biological properties of a new peptide with antimicrobial properties. Arch. Biochem. Biophys. 691: 108487.
    Pubmed
  29. McKenna M. 2013. Antibiotic resistance: the last resort. Nature 499: 394-396.
    Pubmed
  30. Menousek J, Mishra B, Hanke ML, Heim CE, Kielian T, Wang G. 2012. Database screening and in vivo efficacy of antimicrobial peptides against methicillin-resistant Staphylococcus aureus USA300. Int. J. Antimicrob. Agents 39: 402-406.
    Pubmed KoreaMed
  31. Das T, Nath C, Das P, Ghosh K, Logno TA, Debnath P, et al. 2023. High prevalence of ciprofloxacin resistance in Escherichia coli isolated from chickens, humans and the environment: an emerging one health issue. PLoS One 18: e0294043.
    Pubmed KoreaMed
  32. Shariati A, Arshadi M, Khosrojerdi MA, Abedinzadeh M, Ganjalishahi M, Maleki A, et al. 2022. The resistance mechanisms of bacteria against ciprofloxacin and new approaches for enhancing the efficacy of this antibiotic. Front. Public Health 10: 1025633.
    Pubmed KoreaMed
  33. Pletzer D, Mansour SC, Hancock REW. 2018. ynergy between conventional antibiotics and anti-biofilm peptides in a murine, subcutaneous abscess model caused by recalcitrant ESKAPE pathogens. PLoS Pathog. 14: e1007084.
    Pubmed KoreaMed
  34. Lin MF, Lin YY, Lan CY. 2019. A method to assess influence of different medical tubing on biofilm formation by Acinetobacter baumannii. J. Microbiol. Methods 160: 84-86.
    Pubmed
  35. Lin Y, Chang RYK, Britton WJ, Morales S, Kutter E, Chan HK. 2018. Synergy of nebulized phage PEV20 and ciprofloxacin combination against Pseudomonas aeruginosa. Int. J. Pharm. 551: 158-165.
    Pubmed KoreaMed
  36. Rishi P, Vashist T, Sharma A, Kaur A, Kaur A, Kaur N, et al. 2018. Efficacy of designer K11 antimicrobial peptide (a hybrid of melittin, cecropin A1 and magainin 2) against Acinetobacter baumannii-infected wounds. Pathog. Dis. 76. doi: 10.1093/femspd/fty072.
    Pubmed
  37. Powers JPS, Hancock REW. 2003. The relationship between peptide structure and antibacterial activity. Peptides 24: 1681-1691.
    Pubmed
  38. Sharma P, Ayappa KG. A 2022. Molecular dynamics study of antimicrobial peptide interactions with the lipopolysaccharides of the outer bacterial membrane. J. Membr. Biol. 255: 665-675.
    Pubmed
  39. Thakur S, Cattoni DI, Nöllmann M. 2015. The fluorescence properties and binding mechanism of SYTOX green, a bright, low photo-damage DNA intercalating agent. Eur. Biophys. J. 44: 337-348.
    Pubmed
  40. Shagaghi N, Palombo EA, Clayton AHA, Bhave M. 2018. Antimicrobial peptides: biochemical determinants of activity and biophysical techniques of elucidating their functionality. World J. Microbiol. Biotechnol. 34: 62.
    Pubmed
  41. Travkova OG, Moehwald H, Brezesinski G. 2017. The interaction of antimicrobial peptides with membranes. Adv. Colloid Interface Sci. 247: 521-532.
    Pubmed
  42. Allegra E, Titball RW, Carter J, Champion OL. 2018. Galleria mellonella larvae allow the discrimination of toxic and non-toxic chemicals. Chemosphere 198: 469-472.
    Pubmed
  43. Browne N, Heelan M, Kavanagh K. 2013. An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 4: 597-603.
    Pubmed KoreaMed
  44. Wojda I. 2017. Immunity of the greater wax moth Galleria mellonella. Insect Sci. 24: 342-357.
    Pubmed
  45. Nguyen LT, Chau JK, Perry NA, de Boer L, Zaat SAJ, Vogel HJ. 2010. Serum stabilities of short tryptophan- and arginine-rich antimicrobial peptide analogs. PLoS One 5: e12684.
    Pubmed KoreaMed
  46. Jia F, Zhang Y, Wang J, Peng J, Zhao P, Zhang L, et al. 2019. The effect of halogenation on the antimicrobial activity, antibiofilm activity, cytotoxicity and proteolytic stability of the antimicrobial peptide Jelleine-I. Peptides 112: 56-66.
    Pubmed