Single-cell, real-time detection of oxidative stress induced in escherichia coli by the antimicrobial peptide CM15

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 3, 2015, Pages E303-E310

  Choi, Heejun ^a   Yang, Zhilin ^a   Weisshaar, James C ^a,b  

^a Department of Chemistry ^*  (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Antimicrobial peptide; CM15; E. coli; Oxidative stress; Real time ROS assay

Indexed keywords

ANTIMICROBIAL PEPTIDE CM15; HYDROGEN PEROXIDE; MELITTIN; POLYPEPTIDE ANTIBIOTIC AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; ANTIMICROBIAL HYBRID PEPTIDE CM15;

ARTICLE; BACTERIAL MEMBRANE; BREATHING; CELL DAMAGE; CELL MEMBRANE PERMEABILITY; CONCENTRATION (PARAMETERS); CYTOPLASM; DRUG POTENCY; ESCHERICHIA COLI; FLUORESCENCE ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FOLDING; SINGLE CELL ANALYSIS; DRUG EFFECTS; FLUORESCENCE; METABOLISM; MICROBIAL SENSITIVITY TEST;

APOIDEA; ESCHERICHIA COLI; LEPIDOPTERA;

ANTIMICROBIAL CATIONIC PEPTIDES; ESCHERICHIA COLI; FLUORESCENCE; MICROBIAL SENSITIVITY TESTS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84921340438     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417703112     Document Type: Article

References (36)

1. Wimley WC, Hristova K (2011) Antimicrobial peptides: Successes, challenges and unanswered questions. J Membr Biol 239(1-2):27-34.
2. Brogden KA (2005) Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3(3):238-250.
3. Hancock RE, Sahl HG (2013) New strategies and compounds for anti-infective treatment. Curr Opin Microbiol 16(5):519-521.
4. Wenzel M, et al. (2014) Small cationic antimicrobial peptides delocalize peripheral membrane proteins. Proc Natl Acad Sci USA 111(14):E1409-E1418.
5. Schlamadinger DE, Wang Y, McCammon JA, Kim JE (2012) Spectroscopic and computational study of melittin, cecropin A, and the hybrid peptide CM15. J Phys Chem B 116(35):10600-10608.
6. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130(5):797-810.
7. Kohanski MA, Dwyer DJ, Collins JJ (2010) How antibiotics kill bacteria: From targets to networks. Nat Rev Microbiol 8(6):423-435.
8. Liu Y, Imlay JA (2013) Cell death from antibiotics without the involvement of reactive oxygen species. Science 339(6124):1210-1213.
9. Keren I, Wu Y, Inocencio J, Mulcahy LR, Lewis K (2013) Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 339(6124):1213-1216.
10. Ezraty B, et al. (2013) Fe-S cluster biosynthesis controls uptake of aminoglycosides in a ROS-less death pathway. Science 340(6140):1583-1587.
11. Dwyer DJ, et al. (2014) Antibiotics induce redox-related physiological alterations as part of their lethality. Proc Natl Acad Sci USA 111(20):E2100-E2109.
12. Zhao X, Drlica K (2014) Reactive oxygen species and the bacterial response to lethal stress. Curr Opin Microbiol 21C:1-6.
13. Dwyer DJ, Collins JJ, Walker GC (2015) Unraveling the physiological complexities of antibiotic lethality. Annu Rev Pharmacol Toxicol, 10.1146/annurev-pharmtox-010814-124712.
14. Barns KJ, Weisshaar JC (2013) Real-time attack of LL-37 on single Bacillus subtilis cells. Biochim Biophys Acta 1828(6):1511-1520.
15. Rangarajan N, Bakshi S, Weisshaar JC (2013) Localized permeabilization of E. coli membranes by the antimicrobial peptide Cecropin A. Biochemistry 52(38):6584-6594.
16. Sochacki KA, Barns KJ, Bucki R, Weisshaar JC (2011) Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37. Proc Natl Acad Sci USA 108(16):E77-E81.
17. Sargent F (2007) The twin-arginine transport system: Moving folded proteins across membranes. Biochem Soc Trans 35(Pt 5):835-847.
18. Lu HP, Xun L, Xie XS (1998) Single-molecule enzymatic dynamics. Science 282(5395): 1877-1882.
19. Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: Lessons from a model bacterium. Nat Rev Microbiol 11(7):443-454.
20. Bakshi S, Siryaporn A, Goulian M, Weisshaar JC (2012) Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol Microbiol 85(1):21-38.
21. Unden G, Bongaerts J (1997) Alternative respiratory pathways of Escherichia coli: Energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320(3):217-234.
22. Woodmansee AN, Imlay JA (2003) A mechanism by which nitric oxide accelerates the rate of oxidative DNA damage in Escherichia coli. Mol Microbiol 49(1):11-22.
23. Martell JD, et al. (2012) Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat Biotechnol 30(11):1143-1148.
24. Flint DH, Tuminello JF, Emptage MH (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268(30):22369-22376.
25. Imlay JA, Chin SM, Linn S (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240(4852):640-642.
26. Messner KR, Imlay JA (2002) Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J Biol Chem 277(45):42563-42571.
27. Yoshikawa S, Muramoto K, Shinzawa-Itoh K (2011) Proton-pumping mechanism of cytochrome c oxidase. Ann Rev Biophys 40:205-223.
28. Collman JP, et al. (2007) A cytochrome C oxidase model catalyzes oxygen to water reduction under rate-limiting electron flux. Science 315(5818):1565-1568.
29. Schroeder BO, et al. (2011) Reduction of disulphide bonds unmasks potent antimicrobial activity of human β-defensin 1. Nature 469(7330):419-423.
30. Liu W, et al. (2013) Effect of intracellular expression of antimicrobial peptide LL-37 on growth of Escherichia coli strain TOP10 under aerobic and anaerobic conditions. Antimicrob Agents Chemother 57(10):4707-4716.
31. Kashyap DR, et al. (2014) Peptidoglycan recognition proteins kill bacteria by inducing oxidative, thiol, and metal stress. PLoS Pathog 10(7):e1004280.
32. Sochacki KA, Shkel IA, Record MT, Weisshaar JC (2011) Protein diffusion in the periplasm of E. coli under osmotic stress. Biophys J 100(1):22-31.
33. Thiel A, Valens M, Vallet-Gely I, Espéli O, Boccard F (2012) Long-range chromosome organization in E. coli: A site-specific system isolates the Ter macrodomain. PLoS Genet 8(4):e1002672.
34. Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119(3):736-747.
35. Aitken CE, Marshall RA, Puglisi JD (2008) An oxygen scavenging system for improvement of dye stability in single-molecule fluorescence experiments. Biophys J 94(5):1826-1835.
36. Park S, You X, Imlay JA (2005) Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proc Natl Acad Sci USA 102(26):9317-9322.