Single-Cell, Time-Resolved Antimicrobial Effects of a Highly Cationic, Random Nylon-3 Copolymer on Live Escherichia coli

ACS Chemical Biology

Volumn 11, Issue 1, 2016, Pages 113-120

  Choi, Heejun ^a   Chakraborty, Saswata ^a   Liu, Runhui ^a   Gellman, Samuel H ^a   Weisshaar, James C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; COPOLYMER; NYLON; REACTIVE OXYGEN METABOLITE; ANTIMICROBIAL CATIONIC PEPTIDE; POLYMER;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL; CELL MEMBRANE; CELL PERMEABILIZATION; CONTROLLED STUDY; ERYTHROCYTE; ESCHERICHIA COLI; GROWTH INHIBITION; HEMOLYSIS; HYPEROSMOTIC STRESS; MICROBIAL GROWTH; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OUTER MEMBRANE; OXIDATIVE STRESS; PLASMOLYSIS; PRIORITY JOURNAL; CHEMISTRY; DRUG EFFECTS; HUMAN; MICROBIAL SENSITIVITY TEST;

ANTIMICROBIAL CATIONIC PEPTIDES; ERYTHROCYTES; ESCHERICHIA COLI; HUMANS; MICROBIAL SENSITIVITY TESTS; OXIDATIVE STRESS; POLYMERS;

EID: 84954555379     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00547     Document Type: Article

References (37)

1. Hancock, R. E. and Sahl, H. G. (2013) New strategies and compounds for anti-infective treatment Curr. Opin. Microbiol. 16, 519-521 10.1016/j.mib.2013.08.004
2. Afacan, N. J., Yeung, A. T., Pena, O. M., and Hancock, R. E. (2012) Therapeutic potential of host defense peptides in antibiotic-resistant infections Curr. Pharm. Des. 18, 807-819 10.2174/138161212799277617
3. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms Nature 415, 389-395 10.1038/415389a
4. Gallo, R. L. and Hooper, L. V. (2012) Epithelial antimicrobial defence of the skin and intestine Nat. Rev. Immunol. 12, 503-516 10.1038/nri3228
5. Guilhelmelli, F., Vilela, N., Albuquerque, P., Derengowski, L. d. S., Silva-Pereira, I., and Kyaw, C. M. (2013) Antibiotic development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance Front. Microbiol. 4, 353 10.3389/fmicb.2013.00353
6. Brogden, K. A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250 10.1038/nrmicro1098
7. Liu, R., Chen, X., Chakraborty, S., Lemke, J. J., Hayouka, Z., Chow, C., Welch, R. A., Weisblum, B., Masters, K. S., and Gellman, S. H. (2014) Tuning the Biological Activity Profile of Antibacterial Polymers via Subunit Substitution Pattern J. Am. Chem. Soc. 136, 4410-4418 10.1021/ja500367u
8. Chakraborty, S., Liu, R., Hayouka, Z., Chen, X., Ehrhardt, J., Lu, Q., Burke, E., Yang, Y., Weisblum, B., Wong, G. C. L., Masters, K. S., and Gellman, S. H. (2014) Ternary Nylon-3 Copolymers as Host-Defense Peptide Mimics: Beyond Hydrophobic and Cationic Subunits J. Am. Chem. Soc. 136, 14530-14535 10.1021/ja507576a
9. Chakraborty, S., Liu, R., Lemke, J. J., Hayouka, Z., Welch, R. A., Weisblum, B., Masters, K. S., and Gellman, S. H. (2013) Effects of Cyclic vs Acyclic Hydrophobic Subunits on the Chemical Structure and Biological Properties of Nylon-3 Copolymers ACS Macro Lett. 2, 753-756 10.1021/mz400239r
10. Mowery, B. P., Lindner, A. H., Weisblum, B., Stahl, S. S., and Gellman, S. H. (2009) Structure-activity Relationships among Random Nylon-3 Copolymers That Mimic Antibacterial Host-Defense Peptides J. Am. Chem. Soc. 131, 9735-9745 10.1021/ja901613g
11. Epand, R. F., Mowery, B. P., Lee, S. E., Stahl, S. S., Lehrer, R. I., Gellman, S. H., and Epand, R. M. (2008) Dual Mechanism of Bacterial Lethality for a Cationic Sequence-Random Copolymer that Mimics Host-Defense Antimicrobial Peptides J. Mol. Biol. 379, 38-50 10.1016/j.jmb.2008.03.047
12. Mowery, B. P., Lee, S. E., Kissounko, D. A., Epand, R. F., Epand, R. M., Weisblum, B., Stahl, S. S., and Gellman, S. H. (2007) Mimicry of antimicrobial host-defense peptides by random copolymers J. Am. Chem. Soc. 129, 15474-15475 10.1021/ja077288d
13. Choi, H., Yang, Z., and Weisshaar, J. C. (2015) Single-cell, real-time detection of oxidative stress induced in Escherichia coli by the antimicrobial peptide CM15 Proc. Natl. Acad. Sci. U. S. A. 112, E303-E310 10.1073/pnas.1417703112
14. Bakshi, S., Choi, H., Rangarajan, N., Barns, K. J., Bratton, B. P., and Weisshaar, J. C. (2014) Nonperturbative Imaging of Nucleoid Morphology in Live Bacterial Cells during an Antimicrobial Peptide Attack Appl. Environ. Microbiol. 80, 4977-4986 10.1128/AEM.00989-14
15. Bakshi, S., Choi, H., Mondal, J., and Weisshaar, J. C. (2014) Time-dependent effects of transcription- and translation-halting drugs on the spatial distributions of the Escherichia coli chromosome and ribosomes Mol. Microbiol. 94, 871-887 10.1111/mmi.12805
16. Barns, K. J. and Weisshaar, J. C. (2013) Real-time attack of LL-37 on single Bacillus subtilis cells Biochim. Biophys. Acta, Biomembr. 1828, 1511-1520 10.1016/j.bbamem.2013.02.011
17. Rangarajan, N., Bakshi, S., and Weisshaar, J. C. (2013) Localized permeabilization of E. coli membranes by the antimicrobial peptide Cecropin A Biochemistry 52, 6584-6594 10.1021/bi400785j
18. Sochacki, K. A., Barns, K. J., Bucki, R., and Weisshaar, J. C. (2011) Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37 Proc. Natl. Acad. Sci. U. S. A. 108, E77-E81 10.1073/pnas.1101130108
19. Lee, M. W., Chakraborty, S., Schmidt, N. W., Murgai, R., Gellman, S. H., and Wong, G. C. L. (2014) Two interdependent mechanisms of antimicrobial activity allow for efficient killing in nylon-3-based polymeric mimics of innate immunity peptides Biochim. Biophys. Acta, Biomembr. 1838, 2269-2279 10.1016/j.bbamem.2014.04.007
20. Sochacki, K. A., Shkel, I. A., Record, M. T., and Weisshaar, J. C. (2011) Protein Diffusion in the Periplasm of E. coli under Osmotic Stress Biophys. J. 100, 22-31 10.1016/j.bpj.2010.11.044
21. Pilizota, T. and Shaevitz, J. W. (2013) Plasmolysis and Cell Shape Depend on Solute Outer-Membrane Permeability during Hyperosmotic Shock in E. coli Biophys. J. 104, 2733-2742 10.1016/j.bpj.2013.05.011
22. Rojas, E., Theriot, J. A., and Huang, K. (2014) The response of bacterial growth rate to osmotic shock Proc. Natl. Acad. Sci. U. S. A. 111, 7807-7812 10.1073/pnas.1402591111
23. MacMillan, S. V., Alexander, D. A., Culham, D. E., Kunte, H. J., Marshall, E. V., Rochon, D., and Wood, J. M. (1999) The ion coupling and organic substrate specificities of osmoregulatory transporter ProP in Escherichia coli Biochim. Biophys. Acta, Biomembr. 1420, 30-44 10.1016/S0005-2736(99)00085-1
24. Wilks, J. C. and Slonczewski, J. L. (2007) pH of the cytoplasm and periplasm of Escherichia coli: Rapid measurement by green fluorescent protein fluorimetry J. Bacteriol. 189, 5601-5607 10.1128/JB.00615-07
25. + uptake system in Escherichia coli upon hyper-osmotic stress at a low pH FEBS Lett. 447, 144-148 10.1016/S0014-5793(99)00288-4
26. + transport in Escherichia coli K-12 J. Biol. Chem. 252, 1394-1401
27. +-translocating KDP-ATPase from Escherichia coli J. Biol. Chem. 264, 5831-5838
28. + binding sites in the KDP transport ATPase J. Biol. Chem. 270, 6678-6685
29. Spector, J., Zakharov, S., Lill, Y., Sharma, O., Cramer, W. A., and Ritchie, K. (2010) Mobility of BtuB and OmpF in the Escherichia coli outer membrane: implications for dynamic formation of a translocon complex Biophys. J. 99, 3880-3886 10.1016/j.bpj.2010.10.029
30. Housden, N. G., Hopper, J. T. S., Lukoyanova, N., Rodriguez-Larrea, D., Wojdyla, J. A., Klein, A., Kaminska, R., Bayley, H., Saibil, H. R., Robinson, C. V., and Kleanthous, C. (2013) Intrinsically Disordered Protein Threads Through the Bacterial Outer-Membrane Porin OmpF Science 340, 1570-1574 10.1126/science.1237864
31. Wood, J. M. (2015) Bacterial responses to osmotic challenges J. Gen. Physiol. 145, 381-388 10.1085/jgp.201411296
32. Richey, B., Cayley, D. S., Mossing, M. C., Kolka, C., Anderson, C. F., Farrar, T. C., and Record, M. T. (1987) Variability of the Intracellular Ionic Environment of Escherichia coli-Differences between In vitro and In vivo Effects of Ion Concentrations on Protein-DNA Interactions and Gene Expression J. Biol. Chem. 262, 7157-7164
33. Record, M. T., Jr., Anderson, C. F., Mills, P., Mossing, M., and Roe, J. H. (1985) Ions as regulators of protein-nucleic acid interactions in vitro and in vivo Adv. Biophys. 20, 109-135 10.1016/0065-227X(85)90033-4
34. Oliver, P. M., Crooks, J. A., Leidl, M., Yoon, E. J., Saghatelian, A., and Weibel, D. B. (2014) Localization of Anionic Phospholipids in Escherichia coli Cells J. Bacteriol. 196, 3386-3398 10.1128/JB.01877-14
35. Hancock, R. E. W. and Sahl, H.-G. (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 24, 1551-1557 10.1038/nbt1267
36. Neidhardt, F. C., Bloch, P. L., and Smith, D. F. (1974) Culture medium for enterobacteria J. Bacteriol. 119, 736-747
37. Choi, H., Chakraborty, S., Liu, R., Gellman, S. H., and Weisshaar, J. C. (2014) Medium Effects on Minimum Inhibitory Concentrations of Nylon-3 Polymers against E. coli PLoS One 9, e104500 10.1371/journal.pone.0104500