Engineering persister-specific antibiotics with synergistic antimicrobial functions

ACS Nano

Volumn 8, Issue 9, 2014, Pages 8786-8793

  Schmidt, Nathan W ^a   Deshayes, Stephanie ^a   Hawker, Sinead ^a   Blacker, Alyssa ^a   Kasko, Andrea M ^a   Wong, Gerard C L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

aminoglycoside; antibiotics; bacterial resistance; cell penetrating peptide; drug design

Indexed keywords

AMINO ACIDS; ESCHERICHIA COLI; METABOLISM; MOBILE SECURITY;

AMINOGLYCOSIDE ANTIBIOTICS; AMINOGLYCOSIDES; ANTIBIOTIC ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL FUNCTIONS; BACTERIAL RESISTANCE; CELL-PENETRATING PEPTIDE; DRUG DESIGN;

ANTIBIOTICS;

ANTIINFECTIVE AGENT; TOBRAMYCIN;

3T3 CELL LINE; ANIMAL; ANTIBIOTIC RESISTANCE; CELL MEMBRANE PERMEABILITY; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ESCHERICHIA COLI; MOUSE; STAPHYLOCOCCUS AUREUS; SYNTHESIS;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL MEMBRANE PERMEABILITY; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; MICE; NIH 3T3 CELLS; STAPHYLOCOCCUS AUREUS; TOBRAMYCIN;

EID: 84925590102     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn502201a     Document Type: Article

References (53)

1. CDC Threat Report 2013.
2. Dantes, R.; Mu, Y.; Belflower, R.; Aragon, D.; Dumyati, G.; Harrison, L. H.; Lessa, F. C.; Lynfield, R.; Nadle, J.; Petit, S. et al. National Burden of Invasive Methicillin-Resistant Staphylococcus Aureus Infections, United States, 2011 JAMA Int. Med. 2013, 173, 1970-1978
3. Taubes, G. The Bacteria Fight Back Science 2008, 321, 356-361
4. Ochman, H.; Lawrence, J. G.; Groisman, E. A. Lateral Gene Transfer and the Nature of Bacterial Innovation Nature 2000, 405, 299-304
5. Balaban, N. Q.; Merrin, J.; Chait, R.; Kowalik, L.; Leibler, S. Bacterial Persistence as a Phenotypic Switch Science 2004, 305, 1622-1625
6. Lewis, K. Persister Cells, Dormancy and Infectious Disease Nat. Rev. Microbiol. 2007, 5, 48-56
7. Gefen, O.; Gabay, C.; Mumcuoglu, M.; Engel, G.; Balaban, N. Q. Single-Cell Protein Induction Dynamics Reveals a Period of Vulnerability to Antibiotics in Persister Bacteria Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 6145-6149
8. Gefen, O.; Balaban, N. Q. The Importance of Being Persistent: Heterogeneity of Bacterial Populations under Antibiotic Stress FEMS Microbiol. Rev. 2009, 33, 704-717
9. Bigger, J. Treatment of Staphylococcal Infections with Penicillin by Intermittent Sterilisation Lancet 1944, 244, 497-500
10. Keren, I.; Kaldalu, N.; Spoering, A.; Wang, Y.; Lewis, K. Persister Cells and Tolerance to Antimicrobials FEMS Microbiol. Lett. 2004, 230, 13-18
11. Mulcahy, L. R.; Burns, J. L.; Lory, S.; Lewis, K. Emergence of Pseudomonas Aeruginosa Strains Producing High Levels of Persister Cells in Patients with Cystic Fibrosis J. Bacteriol. 2010, 192, 6191-6199
12. Lewis, K. Persister Cells Annu. Rev. Microbiol. 2010, 64, 357-372
13. Vicens, Q.; Westhof, E. Crystal Structure of a Complex between the Aminoglycoside Tobramycin and an Oligonucleotide Containing the Ribosomal Decoding A Site Chem. Biol. 2002, 9, 747-755
14. Fourmy, D.; Recht, M. I.; Blanchard, S. C.; Puglisi, J. D. Structure of the a Site of Escherichia Coli 16s Ribosomal RNA Complexed with an Aminoglycoside Antibiotic Science 1996, 274, 1367
15. Davis, B. D. Mechanism of Bactericidal Action of Aminoglycosides Microbiol. Rev. 1987, 51, 341
16. Allison, K. R.; Brynildsen, M. P.; Collins, J. J. Metabolite-Enabled Eradication of Bacterial Persisters by Aminoglycosides Nature 2011, 473, 216-220
17. Schmidt, N. W.; Wong, G. C. Antimicrobial Peptides and Induced Membrane Curvature: Geometry, Coordination Chemistry, and Molecular Engineering Curr. Opin. Solid State Mater. Sci. 2013, 17, 151-163
18. Brogden, K. A. Antimicrobial Peptides: Pore Formers or Metabolic Inhibitors in Bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250
19. Hurdle, J. G.; O'Neill, A. J.; Chopra, I.; Lee, R. E. Targeting Bacterial Membrane Function: An Underexploited Mechanism for Treating Persistent Infections Nat. Rev. Microbiol. 2011, 9, 62-75
20. Bera, S.; Zhanel, G. G.; Schweizer, F. Design, Synthesis, and Antibacterial Activities of Neomycin-Lipid Conjugates: Polycationic Lipids with Potent Gram-Positive Activity J. Med. Chem. 2008, 51, 6160-6164
21. Dhondikubeer, R.; Bera, S.; Zhanel, G. G.; Schweizer, F. Antibacterial Activity of Amphiphilic Tobramycin J. Antibiot. 2012, 65, 495-498
22. Bryskier, A. Dual B-Lactam-Fluoroquinolone Compounds: A Novel Approach to Antibacterial Treatment Expert Opin. Invest. Drugs 1997, 6, 1479-1499
23. Mishra, A.; Lai, G. H.; Schmidt, N. W.; Sun, V. Z.; Rodriguez, A. R.; Tong, R.; Tang, L.; Cheng, J.; Deming, T. J.; Kamei, D. T. et al. Translocation of HIV Tat Peptide and Analogues Induced by Multiplexed Membrane and Cytoskeletal Interactions Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 16883-16888
24. Schmidt, N. W.; Mishra, A.; Lai, G. H.; Davis, M.; Sanders, L. K.; Tran, D.; Garcia, A.; Tai, K. P.; McCray, P. B., Jr.; Ouellette, A. J. Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization J. Am. Chem. Soc. 2011, 133, 6720-6727
25. Schmidt, N. W.; Lis, M.; Zhao, K.; Lai, G. H.; Alexandrova, A. N.; Tew, G. N.; Wong, G. C. Molecular Basis for Nanoscopic Membrane Curvature Generation from Quantum Mechanical Models and Synthetic Transporter Sequences J. Am. Chem. Soc. 2012, 134, 19207-19216
26. Hu, K.; Schmidt, N. W.; Zhu, R.; Jiang, Y.; Lai, G. H.; Wei, G.; Palermo, E. F.; Kuroda, K.; Wong, G. C.; Yang, L. A Critical Evaluation of Random Copolymer Mimesis of Homogeneous Antimicrobial Peptides Macromolecules 2013, 46, 1908-1915
27. Lehrer, R. I.; Barton, A.; Ganz, T. Concurrent Assessment of Inner and Outer Membrane Permeabilization and Bacteriolysis in E. coli by Multiple-Wavelength Spectrophotometry J. Immunol. Methods 1988, 108, 153-158
28. Asensio, J. L.; Hidalgo, A.; Bastida, A.; Torrado, M.; Corzana, F.; Chiara, J. L.; Garcia-Junceda, E.; Canada, J.; Jimenez-Barbero, J. A Simple Structural-Based Approach to Prevent Aminoglycoside Inactivation by Bacterial Defense Proteins. Conformational Restriction Provides Effective Protection against Neomycin-B Nucleotidylation by Ant4 J. Am. Chem. Soc. 2005, 127, 8278-8279
29. Hanessian, S.; Masse, R.; Capmeau, M. L. Aminoglycoside Antibiotics: Synthesis of 5'-Amino 5'-Deoxyneomycin and 5'-Amino-5'-Deoxyparamomycin J. Antibiot. 1977, 30, 893-896
30. Michael, K.; Tor, Y. Modifying Aminoglycoside Antibiotics. In RNA-Binding Antibiotics; Wallis, R. S. a. M. G., Ed.; Landes Bioscience, 2000.
31. Schwarz, U. S.; Gompper, G. Stability of Inverse Bicontinuous Cubic Phases in Lipid-Water Mixtures Phys. Rev. Lett. 2000, 85, 1472-1475
32. Shearman, G.; Ces, O.; Templer, R.; Seddon, J. Inverse Lyotropic Phases of Lipids and Membrane Curvature J. Phys.: Condens. Matter 2006, 18, S1105
33. Schmidt, N.; Mishra, A.; Lai, G. H.; Wong, G. C. Arginine-Rich Cell-Penetrating Peptides FEBS Lett. 2010, 584, 1806-1813
34. Davis, B. D.; Chen, L. L.; Tai, P. C. Misread Protein Creates Membrane Channels: An Essential Step in the Bactericidal Action of Aminoglycosides Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 6164-6168
35. Mishra, A.; Gordon, V. D.; Yang, L.; Coridan, R.; Wong, G. C. Hiv Tat Forms Pores in Membranes by Inducing Saddle-Splay Curvature: Potential Role of Bidentate Hydrogen Bonding Angew. Chem., Int. Ed. 2008, 47, 2986-2989
36. Llenado, R. A.; Weeks, C. S.; Cocco, M. J.; Ouellette, A. J. Electropositive Charge in A-Defensin Bactericidal Activity: Functional Effects of Lys-for-Arg Substitutions Vary with the Peptide Primary Structure Infect. Immun. 2009, 77, 5035-5043
37. Magnet, S.; Blanchard, J. S. Molecular Insights into Aminoglycoside Action and Resistance Chem. Rev. (Washington, DC, U. S.) 2005, 105, 477-498
38. Kohanski, M. A.; Dwyer, D. J.; Wierzbowski, J.; Cottarel, G.; Collins, J. J. Mistranslation of Membrane Proteins and Two-Component System Activation Trigger Antibiotic-Mediated Cell Death Cell 2008, 135, 679-690
39. Vakulenko, S. B.; Mobashery, S. Versatility of Aminoglycosides and Prospects for Their Future Clin. Microbiol. Rev. 2003, 16, 430-450
40. Taber, H. W.; Mueller, J.; Miller, P.; Arrow, A. Bacterial Uptake of Aminoglycoside Antibiotics Microbiol. Rev. 1987, 51, 439
41. Shah, D.; Zhang, Z.; Khodursky, A. B.; Kaldalu, N.; Kurg, K.; Lewis, K. Persisters: A Distinct Physiological State of E. coli BMC Microbiol. 2006, 6, 53
42. Spoering, A. L.; Lewis, K. Biofilms and Planktonic Cells of Pseudomonas Aeruginosa Have Similar Resistance to Killing by Antimicrobials J. Bacteriol. 2001, 183, 6746-6751
43. Snyder, E.; Dowdy, S. Cell Penetrating Peptides in Drug Delivery Pharm. Res. 2004, 21, 389-393
44. Zorko, M.; Langel, U. Cell-Penetrating Peptides: Mechanism and Kinetics of Cargo Delivery Adv. Drug Delivery Rev. 2005, 57, 529-545
45. Lindgren, M.; Hallbrink, M.; Prochiantz, A.; Langel, U. Cell-Penetrating Peptides Trends Pharmacol. Sci. 2000, 21, 99-103
46. Hsu, C.-H.; Chen, C.; Jou, M.-L.; Lee, A. Y.-L.; Lin, Y.-C.; Yu, Y.-P.; Huang, W.-T.; Wu, S.-H. Structural and DNA-Binding Studies on the Bovine Antimicrobial Peptide, Indolicidin: Evidence for Multiple Conformations Involved in Binding to Membranes and DNA Nucleic Acids Res. 2005, 33, 4053-4064
47. Park, C. B.; Kim, H. S.; Kim, S. C. Mechanism of Action of the Antimicrobial Peptide Buforin II: Buforin Ii Kills Microorganisms by Penetrating the Cell Membrane and Inhibiting Cellular Functions Biochem. Biophys. Res. Commun. 1998, 244, 253-257
48. Yonezawa, A.; Kuwahara, J.; Fujii, N.; Sugiura, Y. Binding of Tachyplesin I to DNA Revealed by Footprinting Analysis: Significant Contribution of Secondary Structure to DNA Binding and Implication for Biological Action Biochemistry 1992, 31, 2998-3004
49. Derossi, D.; Chassaing, G.; Prochiantz, A. Trojan Peptides: The Penetratin System for Intracellular Delivery Trends Cell Biol. 1998, 8, 84-87
50. Derossi, D.; Joliot, A. H.; Chassaing, G.; Prochiantz, A. The Third Helix of the Antennapedia Homeodomain Translocates through Biological Membranes J. Biol. Chem. 1994, 269, 10444-10450
51. Dom, G.; Shaw-Jackson, C.; Matis, C.; Bouffioux, O.; Picard, J. J.; Prochiantz, A.; Mingeot-Leclercq, M. P.; Brasseur, R.; Rezsohazy, R. Cellular Uptake of Antennapedia Penetratin Peptides Is a Two-Step Process in Which Phase Transfer Precedes a Tryptophan-Dependent Translocation Nucleic Acids Res. 2003, 31, 556-561
52. usaxs.xor.aps.anl.gov/staff/ilavsky/nika.html.
53. www.esrf.eu/computing/scientific/FIT2D/.