Structural dynamics influences the antibacterial activity of a cell-penetrating peptide (KFF)
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
08 09 2023
08 09 2023
Historique:
received:
17
03
2023
accepted:
13
07
2023
medline:
11
9
2023
pubmed:
9
9
2023
entrez:
8
9
2023
Statut:
epublish
Résumé
Given the widespread demand for novel antibacterial agents, we modified a cell-penetrating peptide (KFF)
Identifiants
pubmed: 37684254
doi: 10.1038/s41598-023-38745-y
pii: 10.1038/s41598-023-38745-y
pmc: PMC10491836
doi:
Substances chimiques
Cell-Penetrating Peptides
0
Anti-Bacterial Agents
0
Chymotrypsin
EC 3.4.21.1
Endopeptidases
EC 3.4.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14826Informations de copyright
© 2023. Springer Nature Limited.
Références
Avci, F. G., Akbulut, B. S. & Ozkirimli, E. Membrane active peptides and their biophysical characterization. Biomolecules 8, 1–43 (2018).
doi: 10.3390/biom8030077
Sani, M. A. & Separovic, F. How membrane-active peptides get into lipid membranes. Acc. Chem. Res. 49, 1130–1138 (2016).
pubmed: 27187572
doi: 10.1021/acs.accounts.6b00074
Gräslund, A., Madani, F., Lindberg, S., Langel, Ü. & Futaki, S. Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011, 414729 (2011).
pubmed: 21687343
pmcid: 3103903
Heitz, F., Morris, M. C. & Divita, G. Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics. Br. J. Pharmacol. 157, 195–206 (2009).
pubmed: 19309362
pmcid: 2697800
doi: 10.1111/j.1476-5381.2009.00057.x
Lee, H. M. et al. Identification of efficient prokaryotic cell-penetrating peptides with applications in bacterial biotechnology. Commun. Biol. 4, 1–13 (2021).
doi: 10.1038/s42003-021-01726-w
Munyendo, W. L. L., Lv, H., Benza-Ingoula, H., Baraza, L. D. & Zhou, J. Cell penetrating peptides in the delivery of biopharmaceuticals. Biomolecules 2, 187–202 (2012).
pubmed: 24970133
pmcid: 4030843
doi: 10.3390/biom2020187
Yousef, M. et al. Cell-penetrating dabcyl-containing tetraarginines with backbone aromatics as uptake enhancers. Pharmaceutics 15, 141 (2022).
pubmed: 36678772
pmcid: 9864790
doi: 10.3390/pharmaceutics15010141
Lee, H. et al. Conjugation of cell-penetrating peptides to antimicrobial peptides enhances antibacterial activity. ACS Omega 4, 15694–15701 (2019).
pubmed: 31572872
pmcid: 6761801
doi: 10.1021/acsomega.9b02278
Nam, S. H., Park, J. & Koo, H. Recent advances in selective and targeted drug/gene delivery systems using cell-penetrating peptides. Arch. Pharm. Res. 46, 18–34 (2023).
pubmed: 36593377
pmcid: 9807432
doi: 10.1007/s12272-022-01425-y
Eiríksdóttir, E., Konate, K., Langel, Ü., Divita, G. & Deshayes, S. Secondary structure of cell-penetrating peptides controls membrane interaction and insertion. Biochim. Biophys. Acta Biomembr. 1798, 1119–1128 (2010).
doi: 10.1016/j.bbamem.2010.03.005
Gautam, A. et al. CPPsite: A curated database of cell penetrating peptides. Database 2012, 1–7 (2012).
doi: 10.1093/database/bas015
Oikawa, K., Islam, M. M., Horii, Y., Yoshizumi, T. & Numata, K. Screening of a cell-penetrating peptide library in Escherichia coli: Relationship between cell penetration efficiency and cytotoxicity. ACS Omega 3, 16489–16499 (2018).
doi: 10.1021/acsomega.8b02348
Xie, J. et al. Cell-penetrating peptides in diagnosis and treatment of human diseases: From preclinical research to clinical application. Front. Pharmacol. 11, 1–23 (2020).
doi: 10.3389/fphar.2020.00697
Di Pisa, M., Chassaing, G. & Swiecicki, J. M. Translocation mechanism(s) of cell-penetrating peptides: Biophysical studies using artificial membrane bilayers. Biochemistry 54, 194–207 (2015).
pubmed: 25490050
doi: 10.1021/bi501392n
Derakhshankhah, H. & Jafari, S. Cell penetrating peptides: A concise review with emphasis on biomedical applications. Biomed. Pharmacother. 108, 1090–1096 (2018).
pubmed: 30372809
doi: 10.1016/j.biopha.2018.09.097
Desale, K., Kuche, K. & Jain, S. Cell-penetrating peptides (CPPs): An overview of applications for improving the potential of nanotherapeutics. Biomater. Sci. 9, 1153–1188 (2021).
pubmed: 33355322
doi: 10.1039/D0BM01755H
Gori, A. A., Lodigiani, G., Colombarolli, S. G., Bergamaschi, G. & Vitali, A. Cell penetrating peptides: Classification, mechanisms, methods of study and applications. Chem. Med. Chem. 1, e202300236 (2023).
doi: 10.1002/cmdc.202300236
Vaara, M. & Porro, M. Group of peptides that act synergistically with hydrophobic antibiotics against gram-negative enteric bacteria. Antimicrob. Agents Chemother. 40, 1801–1805 (1996).
pubmed: 8843284
pmcid: 163420
doi: 10.1128/AAC.40.8.1801
Wojciechowska, M., Miszkiewicz, J. & Trylska, J. Conformational changes of anoplin, W-MreB1–9, and (KFF)
pubmed: 33352981
pmcid: 7766051
doi: 10.3390/ijms21249672
Bai, H. et al. Targeting RNA polymerase primary σ70 as a therapeutic strategy against methicillin-resistant Staphylococcus aureus by antisense peptide nucleic acid. PLoS ONE 7, 1–10 (2012).
doi: 10.1371/journal.pone.0029886
Kulik, M. et al. Helix 69 of Escherichia coli 23S ribosomal RNA as a peptide nucleic acid target. Biochimie 138, 32–42 (2017).
pubmed: 28396015
doi: 10.1016/j.biochi.2017.04.001
Castillo, J. I., Równicki, M., Wojciechowska, M. & Trylska, J. Antimicrobial synergy between mRNA targeted peptide nucleic acid and antibiotics in E. coli. Bioorg. Med. Chem. Lett. 28, 3094–3098 (2018).
pubmed: 30082123
doi: 10.1016/j.bmcl.2018.07.037
Równicki, M. et al. Vitamin B
doi: 10.1038/s41598-017-08032-8
Wojciechowska, M., Równicki, M., Mieczkowski, A., Miszkiewicz, J. & Trylska, J. Antibacterial peptide nucleic acids: facts and perspectives. Int. J. Mol. Sci. 25, 59 (2020).
Hatamoto, M., Nakai, K., Ohashi, A. & Imachi, H. Sequence-specific bacterial growth inhibition by peptide nucleic acid targeted to the mRNA binding site of 16S rRNA. Appl. Microbiol. Biotechnol. 84, 1161–1168 (2009).
pubmed: 19578844
doi: 10.1007/s00253-009-2099-0
Yavari, N., Goltermann, L. & Nielsen, P. E. Uptake, Stability, and activity of antisense anti- acpP PNA-peptide conjugates in Escherichia coli and the role of SbmA. ACS Chem. Biol. 16, 471–479 (2021).
pubmed: 33684286
doi: 10.1021/acschembio.0c00822
Szabó, I. et al. Redesigning of cell-penetrating peptides to improve their efficacy as a drug delivery system. Pharmaceutics 14, 907 (2022).
pubmed: 35631493
pmcid: 9146218
doi: 10.3390/pharmaceutics14050907
Melikov, K. & Chernomordik, L. V. Arginine-rich cell penetrating peptides: From endosomal uptake to nuclear delivery. Cell. Mol. Life Sci. 62, 2739–2749 (2005).
pubmed: 16231085
doi: 10.1007/s00018-005-5293-y
Nan, Y. H., Park, I. S., Hahm, K. S. & Shin, S. Y. Antimicrobial activity, bactericidal mechanism and LPS-neutralizing activity of the cell-penetrating peptide pVEC and its analogs. J. Pept. Sci. 17, 812–817 (2011).
pubmed: 21956793
doi: 10.1002/psc.1408
Faust, J. E., Yang, P. Y. & Huang, H. W. Action of antimicrobial peptides on bacterial and lipid membranes: A direct comparison. Biophys. J. 112, 1663–1672 (2017).
pubmed: 28445757
pmcid: 5406281
doi: 10.1016/j.bpj.2017.03.003
Budagavi, D. P. & Chugh, A. Antibacterial properties of Latarcin 1 derived cell-penetrating peptides. Eur. J. Pharm. Sci. 115, 43–49 (2018).
pubmed: 29329747
doi: 10.1016/j.ejps.2018.01.015
Zhu, W. L. et al. Design and mechanism of action of a novel bacteria-selective antimicrobial peptide from the cell-penetrating peptide Pep-1. Biochem. Biophys. Res. Commun. 349, 769–774 (2006).
pubmed: 16945333
doi: 10.1016/j.bbrc.2006.08.094
Zhu, W. L., Hahm, K. S. & Shina, S. Y. Cell selectivity and mechanism of action of short antimicrobial peptides designed from the cell-penetrating peptide Pep-1. J. Pept. Sci. 15, 569–575 (2009).
pubmed: 19455552
doi: 10.1002/psc.1145
Shai, Y. Mode of action of membrane active antimicrobial peptides. Pept. Sci. 66, 236–248 (2002).
doi: 10.1002/bip.10260
Mourtada, R. et al. Design of stapled antimicrobial peptides that overcome antibiotic resistance and in vivo toxicity. Nat Biotechnol. 37, 1186–1197 (2019).
pubmed: 31427820
pmcid: 7437984
doi: 10.1038/s41587-019-0222-z
Kim, H. Y., Yum, S. Y., Jang, G. & Ahn, D. R. Discovery of a non-cationic cell penetrating peptide derived from membrane-interacting human proteins and its potential as a protein delivery carrier. Sci. Rep. 5, 1–15 (2015).
Hong, S. Y., Oh, J. E. & Lee, K.-H. Effect of D-amino acid substitution on the stability, the secondary structure, and the activity of membrane-active peptide. Biochem. Pharmacol. 58, 1775–1780 (1999).
pubmed: 10571252
doi: 10.1016/S0006-2952(99)00259-2
Migoń, D., Neubauer, D. & Kamysz, W. Hydrocarbon stapled antimicrobial peptides. Protein J. 37, 2–12 (2018).
pubmed: 29330644
pmcid: 5842273
doi: 10.1007/s10930-018-9755-0
Chapuis, H. et al. Effect of hydrocarbon stapling on the properties of α-helical antimicrobial peptides isolated from the venom of hymenoptera. Amino Acids 43, 2047–2058 (2012).
pubmed: 22526241
doi: 10.1007/s00726-012-1283-1
Blackwell, H. E. & Grubbs, R. H. Highly efficient synthesis of covalently cross-linked peptide helices by ring-closing metathesis. Angew. Chem. Int. Ed. 37, 3281–3284 (1998).
doi: 10.1002/(SICI)1521-3773(19981217)37:23<3281::AID-ANIE3281>3.0.CO;2-V
Lau, Y. H., De Andrade, P., Wu, Y. & Spring, D. R. Peptide stapling techniques based on different macrocyclisation chemistries. Chem. Soc. Rev. 44, 91–102 (2015).
pubmed: 25199043
doi: 10.1039/C4CS00246F
You, Y. H., Liu, H. Y., Zhu, Y. Z. & Zheng, H. Rational design of stapled antimicrobial peptides. Amino Acids 55, 421–442 (2023).
pubmed: 36781451
doi: 10.1007/s00726-023-03245-w
Walensky, L. D. & Bird, G. H. Hydrocarbon-stapled peptides: Principles, practice, and progress. J. Med. Chem. 57, 6275–6288 (2014).
pubmed: 24601557
pmcid: 4136684
doi: 10.1021/jm4011675
Bird, G. H., Christian Crannell, W. & Walensky, L. D. Chemical synthesis of hydrocarbon-stapled peptides for protein interaction research and therapeutic targeting. Curr. Protoc. Chem. Biol. 3, 99–117 (2011).
pubmed: 23801563
pmcid: 4879976
doi: 10.1002/9780470559277.ch110042
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. 40, 1414–1419 (2017).
pubmed: 29075946
doi: 10.1007/s12272-017-0963-5
Mourtada, R. et al. Design of stapled antimicrobial peptides that are stable, nontoxic and kill antibiotic-resistant bacteria in mice. Nat. Biotechnol. 37, 1186–1197 (2019).
pubmed: 31427820
pmcid: 7437984
doi: 10.1038/s41587-019-0222-z
Wojciechowska, M., Macyszyn, J., Miszkiewicz, J., Grzela, R. & Trylska, J. Stapled anoplin as an antibacterial agent. Front. Microbiol. 12, 772038 (2021).
pubmed: 34966367
pmcid: 8710804
doi: 10.3389/fmicb.2021.772038
Stawikowski, G. B. F. M. Introduction to peptide synthesis. Curr. Protoc. Protein Sci. 26, 1–17 (2002).
Kaiser, E., Colescott, R. L., Bossinger, C. D. & Cook, P. I. Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides. Anal. Biochem. 34, 595–598 (1970).
pubmed: 5443684
doi: 10.1016/0003-2697(70)90146-6
Miles, A. J., Ramalli, S. G. & Wallace, B. A. DichroWeb, a website for calculating protein secondary structure from circular dichroism spectroscopic data. Protein Sci. 31, 37–46 (2022).
pubmed: 34216059
doi: 10.1002/pro.4153
Whitmore, L. & Wallace, B. A. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases. Biopolymers 89, 392–400 (2008).
pubmed: 17896349
doi: 10.1002/bip.20853
Abdul-Gader, A., Miles, A. J. & Wallace, B. A. A reference dataset for the analyses of membrane protein secondary structures and transmembrane residues using circular dichroism spectroscopy. Bioinformatics 27, 1630–1636 (2011).
pubmed: 21505036
doi: 10.1093/bioinformatics/btr234
Case, D. A. et al. Amber 2020 (University of California, 2020).
Khoury, G. A. et al. Forcefield-NCAA: Ab initio charge parameters to aid in the discovery and design of therapeutic proteins and peptides with unnatural amino acids and their application to complement inhibitors of the compstatin family. ACS Synth. Biol. 3, 855–869 (2014).
pubmed: 24932669
pmcid: 4277759
doi: 10.1021/sb400168u
Cheng, X., Jo, S., Lee, H. S., Klauda, J. B. & Im, W. CHARMM-GUI micelle builder for pure/mixed micelle and protein/micelle complex systems. J. Chem. Inf. Model. 53, 2171–2180 (2013).
pubmed: 23865552
doi: 10.1021/ci4002684
Allouche, A. Software news and updates gabedit: A graphical user interface for computational chemistry softwares. J. Comput. Chem. 32, 174–182 (2012).
doi: 10.1002/jcc.21600
Turro, N. J. & Yekta, A. Luminescent probes for detergent solutions: A simple procedure for determination of the mean aggregation number of micelles. J. Am. Chem. Soc 100, 5951–5952 (1978).
doi: 10.1021/ja00486a062
Croonen, Y. et al. Influence of salt, detergent concentration, and temperature on the fluorescence quenching of 1-methylpyrene in sodium dodecyl sulfate with m-dicyanobenzene. J. Phys. Chem. 87, 1426–1431 (1983).
doi: 10.1021/j100231a029
Bales, B. L., Messina, L., Vidal, A., Peric, M. & Nascimento, O. R. Precision relative aggregation number determinations of SDS micelles using a spin probe. A model of micelle surface hydration. J. Phys. Chem. B 102, 10347–10358 (1998).
doi: 10.1021/jp983364a
Palazzesi, F., Calvaresi, M. & Zerbetto, F. A molecular dynamics investigation of structure and dynamics of SDS and SDBS micelles. Soft Matter 7, 9148–9156 (2011).
doi: 10.1039/c1sm05708a
Maier, J. A. et al. ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. J. Chem. Theory Comput. 11, 3696–3713 (2015).
pubmed: 26574453
pmcid: 4821407
doi: 10.1021/acs.jctc.5b00255
Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926–935 (1983).
doi: 10.1063/1.445869
Joung, I. S. & Cheatham, T. E. Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B 112, 9020–9041 (2008).
pubmed: 18593145
pmcid: 2652252
doi: 10.1021/jp8001614
Homeyer, N., Horn, A. H. C., Lanig, H. & Sticht, H. AMBER force-field parameters for phosphorylated amino acids in different protonation states: Phosphoserine, phosphothreonine, phosphotyrosine, and phosphohistidine. J. Mol. Model. 12, 281–289 (2006).
pubmed: 16240095
doi: 10.1007/s00894-005-0028-4
Vanommeslaeghe, K. et al. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J. Comput. Chem. 31, 671–690 (2010).
pubmed: 19575467
pmcid: 2888302
doi: 10.1002/jcc.21367
Hopkins, C. W., Le Grand, S., Walker, R. C. & Roitberg, A. E. Long-time-step molecular dynamics through hydrogen mass repartitioning. J. Chem. Theory Comput. 11, 1864–1874 (2015).
pubmed: 26574392
doi: 10.1021/ct5010406
Kabsch, C. S. W. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Sing. Med. J. 12, 2577–2637 (1983).
Roe, D. R. & Cheatham, T. E. PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. J. Chem. Theory Comput. 9, 3084–3095 (2013).
pubmed: 26583988
doi: 10.1021/ct400341p
Hunter, J. D. Matplotlib: A 2D graphics environment. Comput. Sci. Eng. 9, 90–95 (2007).
doi: 10.1109/MCSE.2007.55
Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 7855, 33–38 (1996).
doi: 10.1016/0263-7855(96)00018-5
Zhong, C. et al. Antimicrobial peptides conjugated with fatty acids on the side chain of D-amino acid promises antimicrobial potency against multidrug-resistant bacteria. Eur. J. Pharm. Sci. 141, 105123 (2020).
pubmed: 31676352
doi: 10.1016/j.ejps.2019.105123
Merkler, D. J. C-terminal amidated peptides: Production by the in vitro enzymic amidation of glycine-extended peptides and the importance of the amide to bioactivity. Chem. Inform. 25, 450–456 (2010).
Toniolo, C., Polese, A., Formaggio, F., Crisma, M. & Kamphuis, J. Circular dichroism spectrum of a peptide 3
doi: 10.1021/ja9537383
Watson, R. M. et al. Conformational changes in pediocin AcH upon vesicle binding and approximation of the membrane-bound structure in detergent micelles. Biochemistry 40, 14037–14046 (2001).
pubmed: 11705396
doi: 10.1021/bi011031p
Dorovkov, M. V., Kostyukova, A. S. & Ryazanov, A. G. Phosphorylation of annexin A1 by TRPM7 kinase: A switch regulating the induction of an α-helix. Biochemistry 50, 2187–2193 (2011).
pubmed: 21280599
doi: 10.1021/bi101963h
Doig, A. J., Macarthur, M. W., Stapley, B. J. & Thornton, J. M. Structures of N-termini of helices in proteins. Protein Sci. 6, 147–155 (1997).
pubmed: 9007987
pmcid: 2143508
doi: 10.1002/pro.5560060117
Czapinska, H. & Otlewski, J. Structural and energetic determinants of the S
pubmed: 10102985
doi: 10.1046/j.1432-1327.1999.00160.x
Schafmeister, C. E., Po, J. & Verdine, G. L. An all-hydrocarbon cross-linking system for enhancing the helicity and metabolic stability of peptides. J. Am. Chem. Soc. 122, 5891–5892 (2000).
doi: 10.1021/ja000563a
Malanovic, N. & Lohner, K. Gram-positive bacterial cell envelopes: The impact on the activity of antimicrobial peptides. Biochim. Biophys. Acta Biomembr. 1858, 936–946 (2016).
doi: 10.1016/j.bbamem.2015.11.004
Łoś, J. M., Łoś, M., Wȩgrzyn, A. & Wȩgrzyn, G. Hydrogen peroxide-mediated induction of the Shiga toxin-converting lambdoid prophage ST2-8624 in Escherichia coli O157:H7. FEMS Immunol. Med. Microbiol. 58, 322–329 (2010).
pubmed: 20070366
doi: 10.1111/j.1574-695X.2009.00644.x
Hrabák, J. et al. International clones of Klebsiella pneumoniae and Escherichia coli with extended-spectrum β-lactamases in a Czech Hospital. J. Clin. Microbiol. 47, 3353–3357 (2009).
pubmed: 19710276
pmcid: 2756902
doi: 10.1128/JCM.00901-09
29213 @ www.atcc.org . https://www.atcc.org/products/29213 .
baa-1720 @ www.atcc.org . https://www.atcc.org/products/baa-1720 .
27853 @ www.atcc.org . https://www.atcc.org/products/27853 .
Schoch, C. L. et al. NCBI taxonomy: A comprehensive update on curation, resources and tools. Database 2020, 1–21 (2020).
doi: 10.1093/database/baaa062
Li, B. et al. Colistin resistance gene mcr-1 mediates cell permeability and resistance to hydrophobic antibiotics. Front. Microbiol. 10, 1–7 (2020).
doi: 10.3389/fmicb.2019.03015
Krishnamurthy, M. et al. Enhancing the antibacterial activity of polymyxins using a nonantibiotic drug. Infect. Drug Resist. 12, 1393–1405 (2019).
pubmed: 31239720
pmcid: 6555264
doi: 10.2147/IDR.S196874
Olaitan, A. O., Morand, S. & Rolain, J. M. Mechanisms of polymyxin resistance: Acquired and intrinsic resistance in bacteria. Front. Microbiol. 5, 1–18 (2014).
doi: 10.3389/fmicb.2014.00643
Henriques, S. T., Melo, M. N. & Castanho, M. A. R. B. Cell-penetrating peptides and antimicrobial peptides: How different are they?. Biochem. J. 399, 1–7 (2006).
pubmed: 16956326
pmcid: 1570158
doi: 10.1042/BJ20061100
Bahnsen, J. S., Franzyk, H., Sandberg-Schaal, A. & Nielsen, H. M. Antimicrobial and cell-penetrating properties of penetratin analogs: Effect of sequence and secondary structure. Biochim. Biophys. Acta Biomembr. 1828, 223–232 (2013).
doi: 10.1016/j.bbamem.2012.10.010
Splith, K. & Neundorf, I. Antimicrobial peptides with cell-penetrating peptide properties and vice versa. Eur. Biophys. J. 40, 387–397 (2011).
pubmed: 21336522
doi: 10.1007/s00249-011-0682-7