Antimicrobial activity of the recombinant peptide Melittin-Thanatin with three glycine to tryptophan mutations

References

• World Health Organization. Prioritization of pathogens to guide discovery, research and development of new antibiotics for drug resistant bacterial infections, including tuberculosis. Available at: https://www.who.int/publications/i/item/WHO-EMP-IAU-2017.12.
   Google Scholar
• Lee, J. K.; Luchian, T.; Park, Y. New Antimicrobial Peptide Kills Drug-resistant Pathogens without Detectable Resistance. Oncotarget. 2018, 9, 15616–15634. DOI: 10.18632/oncotarget.24582.
   PubMedGoogle Scholar
• Flórez-Castillo, J. M.; Rondón-Villareal, P.; Ropero-Vega, J. L.; Mendoza-Espinel, S. Y.; Moreno-Amézquita, J. A.; Méndez-Jaimes, K. D.; Farfán-García, A. E.; Gómez-Rangel, S. Y.; Gómez-Duarte, O. G. Ib-M6 Antimicrobial Peptide: Antibacterial Activity against Clinical Isolates of Escherichia coli and Molecular Docking. Antibiotics. 2020, 9, 79. DOI: 10.3390/antibiotics9020079.
   Google Scholar
• Almaaytah, A.; Qaoud, M. T.; Khalil Mohammed, G.; Abualhaijaa, A.; Knappe, D.; Hoffmann, R.; Al-Balas, Q. Antimicrobial and Antibiofilm Activity of up-5, an Ultrashort Antimicrobial Peptide Designed Using Only Arginine and Biphenylalanine. Pharmaceuticals, 2018, 11(1), 1–18. DOI: 10.3390/ph11010003.
   Google Scholar
• Haney, E. F.; Straus, S. K.; Hancock, R. E. W. Reassessing the Host Defense Peptide Landscape. Front. Chem. 2019, 7, 43.
   PubMed Web of Science ®Google Scholar
• Lyu, Y.; Yang, Y.; Lyu, X.; Dong, N.; Shan, A. Antimicrobial Activity, Improved Cell Selectivity and Mode of Action of Short PMAP-36-derived Peptides against Bacteria and Candida. Sci. Rep. 2016, 6, 27258. DOI: 10.1038/srep27258.
   PubMed Web of Science ®Google Scholar
• Hsieh, IN.; Hartshorn, K. L. The Role of Antimicrobial Peptides in Influenza Virus Infection and Their Potential as Antiviral and Immunomodulatory Therapy. Pharmaceuticals. 2016, 9, 53. DOI: 10.3390/ph9030053.
   Google Scholar
• Tanaka, T.; Rahman, M. M.; Battur, B.; Boldbaatar, D.; Liao, M.; Umemiya-Shirafuji, R.; Xuan, X.; Fujisaki, K. Parasiticidal Activity of Human Alpha-defensin-5 against Toxoplasma gondii. In Vitro Cell. Dev. Biol. Anim. 2010, 46, 560–565. DOI: 10.1007/s11626-009-9271-9.
   PubMed Web of Science ®Google Scholar
• Vaezi, Z.; Bortolotti, A.; Luca, V.; Perilli, G.; Mangoni, M. L.; Khosravi-Far, R.; Bobone, S.; Stella, L. Aggregation Determines the Selectivity of Membrane-active Anticancer and Antimicrobial Peptides: The Case of killerFLIP. Biochim. Biophys. Acta. Biomembr. 2020, 1862, 183107. DOI: 10.1016/j.bbamem.2019.183107.
   PubMed Web of Science ®Google Scholar
• Luo, Y.; Song, Y. Mechanism of Antimicrobial Peptides: Antimicrobial, Anti-inflammatory and Antibiofilm Activities. Int J Mol Sci., 2021, 22(21), 1–20. DOI: 10.3390/ijms222111401.
   Google Scholar
• Wang, J.; Zhong, W.; Lin, D.; Xia, F.; Wu, W.; Zhang, H.; Lv, L.; Liu, S.; He, J. Antimicrobial Peptides Derived from Fusion Peptides of Influenza a Viruses, a Promising Approach to Designing Potent Antimicrobial Agents. Chem. Biol. Drug Des. 2015, 86, 487–495. DOI: 10.1111/cbdd.12511.
   PubMed Web of Science ®Google Scholar
• Carmona, G.; Rodriguez, A.; Juarez, D.; Corzo, G.; Villegas, E. Improved Protease Stability of the Antimicrobial Peptide Pin2 Substituted with D-Amino Acids. Protein J. 2013, 32, 456–466. DOI: 10.1007/s10930-013-9505-2.
   PubMed Web of Science ®Google Scholar
• Sieprawska-Lupa, M.; Mydel, P.; Krawczyk, K.; Wójcik, K.; Puklo, M.; Lupa, B.; Suder, P.; Silberring, J.; Reed, M.; Pohl, J.; et al. Degradation of Human Antimicrobial Peptide LL-37 by Staphylococcus aureus-derived Proteinases. Antimicrob. Agents Chemother. 2004, 48, 4673–4679. DOI: 10.1128/AAC.48.12.4673-4679.2004.
   PubMed Web of Science ®Google Scholar
• Gao, Y.; Li, D.; Liu, S.; Zhang, L. Garviecin LG34, a Novel Bacteriocin Produced by Lactococcus garvieae Isolated from Traditional Chinese Fermented Cucumber. Food Control. 2015, 50, 896–900. DOI: 10.1016/j.foodcont.2014.10.040.
   Web of Science ®Google Scholar
• Habermann, E. Bee and Wasp Venoms. Science. 1972, 177, 314–322. DOI: 10.1126/science.177.4046.314.
   PubMed Web of Science ®Google Scholar
• Guha, S.; Ferrie, R. P.; Ghimire, J.; Ventura, C. R.; Wu, E.; Sun, L.; Kim, S. Y.; Wiedman, G. R.; Hristova, K.; Wimley, W. C. Applications and Evolution of Melittin, the Quintessential Membrane Active Peptide. Biochem. Pharmacol. 2021, 193, 114769. DOI: 10.1016/j.bcp.2021.114769.
   PubMed Web of Science ®Google Scholar
• Jenssen, H.; Hamill, P.; Hancock, R. E. Peptide Antimicrobial Agents. Clin. Microbiol. Rev. 2006, 19, 491–511. DOI: 10.1128/CMR.00056-05.
   PubMed Web of Science ®Google Scholar
• Li, J.; Koh, J. J.; Liu, S.; Lakshminarayanan, R.; Verma, C. S.; Beuerman, R. W. Membrane Active Antimicrobial Peptides: Translating Mechanistic Insights to Design. Front. Neurosci. 2017, 11, 73.
   PubMed Web of Science ®Google Scholar
• Lohner, K. Membrane-active Antimicrobial Peptides as Template Structures for Novel Antibiotic Agents. Curr. Top. Med. Chem. 2017, 17, 508–519. DOI: 10.2174/1568026616666160713122404.
   PubMed Web of Science ®Google Scholar
• Dash, R.; Bhattacharjya, S. Thanatin: An Emerging Host Defense Antimicrobial Peptide with Multiple Modes of Action. Int. J. Mol. Sci. 2021, 22(4), 1–13. DOI: 10.3390/ijms22041522.
   Web of Science ®Google Scholar
• Boman, H. G.; Wade, D.; Boman, I. A.; Wåhlin, B.; Merrifield, R. B. Antibacterial and Antimalarial Properties of Peptides That Are Cecropin-Melittin Hybrids. FEBS Lett. 1989, 259, 103–106. DOI: 10.1016/0014-5793(89)81505-4.
   PubMed Web of Science ®Google Scholar
• Deslouches, B.; Steckbeck, J. D.; Craigo, J. K.; Doi, Y.; Mietzner, T. A.; Montelaro, R. C. Rational Design of Engineered Cationic Antimicrobial Peptides Consisting Exclusively of Arginine and Tryptophan, and Their Activity against Multidrug-resistant Pathogens. Antimicrob. Agents Chemother. 2013, 57, 2511–2521. DOI: 10.1128/AAC.02218-12.
   PubMed Web of Science ®Google Scholar
• Jiang, X.; Qian, K.; Liu, G.; Sun, L.; Zhou, G.; Li, J.; Fang, X.; Ge, H.; Lv, Z. Design and Activity Study of a Melittin-Thanatin Hybrid Peptide. AMB Exp. 2019, 9, 14. DOI: 10.1186/s13568-019-0739-z.
   PubMed Web of Science ®Google Scholar
• Yu, H. Y.; Huang, K. C.; Yip, B. S.; Tu, C. H.; Chen, H. L.; Cheng, H. T.; Cheng, J. W. Rational Design of Tryptophan-rich Antimicrobial Peptides with Enhanced Antimicrobial Activities and Specificities. Chembiochem. 2010, 11, 2273–2282. DOI: 10.1002/cbic.201000372.
   PubMed Web of Science ®Google Scholar
• Ji, S.; Li, W.; Baloch, A. R.; Wang, M.; Li, H.; Cao, B.; Zhang, H. Efficient Biosynthesis of a Cecropin A-Melittin Mutant in Bacillus subtilis WB700. Sci. Rep. 2017, 7, 40587. DOI: 10.1038/srep40587.
   PubMed Web of Science ®Google Scholar
• Gill, S. C.; von Hippel, P. H. Calculation of Protein Extinction Coefficients from Amino Acid Sequence Data. Anal. Biochem. 1989, 182, 319–326. DOI: 10.1016/0003-2697(89)90602-7.
   PubMed Web of Science ®Google Scholar
• Wu, M.; Hancock, R. E. Interaction of the Cyclic Antimicrobial Cationic Peptide Bactenecin with the Outer and Cytoplasmic Membrane. J. Biol. Chem. 1999, 274, 29–35. DOI: 10.1074/jbc.274.1.29.
   PubMed Web of Science ®Google Scholar
• Wiegand, I.; Hilpert, K.; Hancock, R. E. Agar and Broth Dilution Methods to Determine the Minimal Inhibitory Concentration (MIC) of Antimicrobial Substances. Nat. Protoc. 2008, 3, 163–175. DOI: 10.1038/nprot.2007.521.
   PubMed Web of Science ®Google Scholar
• Dash, P.; Ghosh, G. Amino Acid Profiling and Antimicrobial Activity of Cucurbita moschata and Lagenaria siceraria Seed Protein Hydrolysates. Nat. Prod. Res. 2018, 32, 2050–2053. DOI: 10.1080/14786419.2017.1359174.
   PubMed Web of Science ®Google Scholar
• Low, A. G. The Activity of Pepsin, Chymotrypsin and Trypsin during 24 h Periods in the Small Intestine of Growing Pigs. Br. J. Nutr. 1982, 48, 147–159. DOI: 10.1079/bjn19820097.
   PubMed Web of Science ®Google Scholar
• Ji, S.; Li, W.; Zhang, L.; Zhang, Y.; Cao, B. Cecropin A-Melittin Mutant with Improved Proteolytic Stability and Enhanced Antimicrobial Activity against Bacteria and Fungi Associated with Gastroenteritis in Vitro. Biochem. Biophys. Res. Commun. 2014, 451, 650–655. DOI: 10.1016/j.bbrc.2014.08.044.
   PubMed Web of Science ®Google Scholar
• Chen, R. F.; Knutson, J. R. Mechanism of Fluorescence Concentration Quenching of Carboxyfluorescein in Liposomes: Energy Transfer to Nonfluorescent Dimers. Anal. Biochem. 1988, 172, 61–77. DOI: 10.1016/0003-2697(88)90412-5.
   PubMed Web of Science ®Google Scholar
• Turner, J.; Cho, Y.; Dinh, N. N.; Waring, A. J.; Lehrer, R. I. Activities of LL-37, a Cathelin-associated Antimicrobial Peptide of Human Neutrophils. Antimicrob. Agents Chemother. 1998, 42, 2206–2214. DOI: 10.1128/AAC.42.9.2206.
   PubMed Web of Science ®Google Scholar
• Greenfield, N. J. Using Circular Dichroism Spectra to Estimate Protein Secondary Structure. Nat. Protoc. 2006, 1, 2876–2890. DOI: 10.1038/nprot.2006.202.
   PubMed Web of Science ®Google Scholar
• Kumar, P.; Kizhakkedathu, J. N.; Straus, S. K. Antimicrobial Peptides: Diversity, Mechanism of Action and Strategies to Improve the Activity and Biocompatibility in Vivo. Biomolecules. 2018, 8, 4. DOI: 10.3390/biom8010004.
   PubMed Web of Science ®Google Scholar
• Joodaki, F.; Martin, L. M.; Greenfield, M. L. Computational Study of Helical and Helix-hinge-helix Conformations of an Anti-microbial Peptide in Solution by Molecular Dynamics and Vibrational Analysis. J. Phys. Chem. B. 2021, 125, 703–721.,
   PubMed Web of Science ®Google Scholar
• Yub Shin, S.; Kang, J. H.; Lee, D. G. Influences of Hinge Region of a Systhetic Antimicrobial Peptide, Cecropin A(1-13)-Melittin(1-13) Hybrid on Antibiotic Activity. Bull Korean Chem Soc, 1999, 20(9), 1078–1084.
   Google Scholar
• Lee, J. K.; Park, S. C.; Hahm, K. S.; Park, Y. A Helix-PXXP-helix Peptide with Antibacterial Activity without Cytotoxicity against MDRPA-infected Mice. Biomaterials. 2014, 35, 1025–1039. DOI: 10.1016/j.biomaterials.2013.10.035.
   PubMed Web of Science ®Google Scholar
• Saravanan, R.; Bhunia, A.; Bhattacharjya, S. Micelle-bound Structures and Dynamics of the Hinge Deleted Analog of Melittin and Its Diastereomer: Implications in Cell Selective Lysis by D-amino Acid Containing Antimicrobial Peptides. Biochim. Biophys. Acta. 2010, 1798, 128–139. DOI: 10.1016/j.bbamem.2009.07.014.
   PubMed Web of Science ®Google Scholar
• Zhang, Q. Y.; Yan, Z. B.; Meng, Y. M.; Hong, X. Y.; Shao, G.; Ma, J. J.; Cheng, X. R.; Liu, J.; Kang, J.; Fu, C. Y. Antimicrobial Peptides: Mechanism of Action, Activity and Clinical Potential. Mil. Med. Res. 2021, 8, 48.
   PubMed Web of Science ®Google Scholar
• Chou, S.; Shao, C.; Wang, J.; Shan, A.; Xu, L.; Dong, N.; Li, Z. Short, Multiple-stranded β-Hairpin Peptides Have Antimicrobial Potency with High Selectivity and Salt Resistance. Acta Biomater. 2016, 30, 78–93. DOI: 10.1016/j.actbio.2015.11.002.
   PubMed Web of Science ®Google Scholar
• Garcia-Fulgueiras, A.; Sánchez, S.; Guillén, J. J.; Marsilla, B.; Aladueña, A.; Navarro, C. A Large Outbreak of Shigella sonnei Gastroenteritis Associated with Consumption of Fresh Pasteurised Milk Cheese. Eur. J. Epidemiol. 2001, 17, 533–538.
   PubMed Web of Science ®Google Scholar
• Yau, W. M.; Wimley, W. C.; Gawrisch, K.; White, S. H. The Preference of Tryptophan for Membrane Interfaces. Biochemistry. 1998, 37, 14713–14718. DOI: 10.1021/bi980809c.
   PubMed Web of Science ®Google Scholar
• Arias, M.; Nguyen, L. T.; Kuczynski, A. M.; Lejon, T.; Vogel, H. J. Position-dependent Influence of the Three Trp Residues on the Membrane Activity of the Antimicrobial Peptide, Tritrpticin. Antibiotics. 2014, 3, 595–616. DOI: 10.3390/antibiotics3040595.
   Google Scholar
• Bi, X.; Wang, C.; Dong, W.; Zhu, W.; Shang, D. Antimicrobial Properties and Interaction of Two Trp-substituted Cationic Antimicrobial Peptides with a Lipid Bilayer. J. Antibiot. 2014, 67, 361–368. DOI: 10.1038/ja.2014.4.
   PubMed Web of Science ®Google Scholar
• Evans, D. F.; Pye, G.; Bramley, R.; Clark, A. G.; Dyson, T. J.; Hardcastle, J. D. Measurement of Gastrointestinal pH Profiles in Normal Ambulant Human Subjects. Gut. 1988, 29, 1035–1041. DOI: 10.1136/gut.29.8.1035.
   PubMed Web of Science ®Google Scholar
• Luong, H. X.; Kim, D. H.; Lee, B. J.; Kim, Y. W. Antimicrobial Activity and Stability of Stapled Helices of Polybia-MP1. Arch. Pharm. Res. 2017, 40, 1414–1419.
   PubMed Web of Science ®Google Scholar
• Kocourková, L.; Novotná, P.; Čujová, S.; Čeřovský, V.; Urbanová, M.; Setnička, V. Conformational Study of Melectin and Antapin Antimicrobial Peptides in Model Membrane Environments. Spectrochim. Acta. A Mol. Biomol. Spectrosc. 2017, 170, 247–255. DOI: 10.1016/j.saa.2016.07.015.
   PubMed Web of Science ®Google Scholar