Tackling vancomycin-resistant bacteria with 'lipophilic-vancomycin-carbohydrate conjugates'

Journal of Antibiotics

Volumn 68, Issue 5, 2015, Pages 302-312

  Yarlagadda, Venkateswarlu ^a   Konai, Mohini M ^a   Manjunath, Goutham B ^a   Ghosh, Chandradhish ^a   Haldar, Jayanta ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DALBAVANCIN; GLYCOCONJUGATE; TELAVANCIN; UNCLASSIFIED DRUG; VANCOMYCIN; VANCOMYCIN ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN ALPHA 1CYCLIC GLUCOSE 4ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN BETA 1CYCLIC GALACTOSE 4ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN BETA 1CYCLIC GLUCOSE 4ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN C10 BETA 1CYCLIC GLUCOSE 4ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN C12 BETA 1CYCLIC GLUCOSE 4ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN C8 BETA 1CYCLIC GLUCOSE 4ACYCLIC GLUCOSE CONJUGATE; VANCOMYCIN CYCLIC GLUCOSE CONJUGATE; VANCOMYCIN DERIVATIVE; ANTIINFECTIVE AGENT; CARBOHYDRATE; PEPTIDE; PROTEIN BINDING;

ALKYLATION; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BINDING AFFINITY; CONTROLLED STUDY; DRUG BINDING; HYDROGEN BOND; LIPOPHILICITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ULTRAVIOLET SPECTROSCOPY; VANCOMYCIN RESISTANT ENTEROCOCCUS; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DRUG EFFECTS; ENTEROCOCCUS; MICROBIAL SENSITIVITY TEST; SYNTHESIS;

BACTERIA (MICROORGANISMS); POSIBACTERIA;

ANTI-BACTERIAL AGENTS; CARBOHYDRATE CONFORMATION; CARBOHYDRATES; ENTEROCOCCUS; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; PEPTIDES; PROTEIN BINDING; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84930196162     PISSN: 00218820     EISSN: 18811469     Source Type: Journal    
DOI: 10.1038/ja.2014.144     Document Type: Article

References (52)

1. Taubes, G. The bacteria fight back. Science 321, 356-361 (2008).
2. Bush, K.et al. Tackling antibiotic resistance. Nat. Rev. Microbiol. 9, 894-896 (2011).
3. Wenzel, R. P., Edmond, M. B. Managing antibiotic resistance. N. Engl. J. Med. 343, 1961-1963 (2000).
4. Kahne, D., Leimkuhler, C., Lu, W., Walsh, C. T. Glycopeptide and lipoglycopeptide antibiotics. Chem. Rev. 105, 425-448 (2005).
5. Yang, Z., Vorpagel, E. R., Laskin, J. Experimental and theoretical studies of the structures and interactions of vancomycin antibiotics with cell wall analogues. J. Am. Chem. Soc. 130, 13013-13022 (2008).
6. Hiramatsu, K. Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect. Dis. 1, 147-155 (2001).
7. McComas, C. C., Crowley, B. M., Boger, D. L. Partitioning the loss in vancomycin binding affinity for D-Ala-D-Lac into lost H-bond and repulsive lone pair contributions. J. Am. Chem. Soc. 125, 9314-9315 (2003).
8. Walsh, C. T., Fisher, S. L., Park, I. S., Prahalad, M., Wu, Z. Bacterial resistance to vancomycin: five genes and one missing hydrogen bond tell the story. Chem. Biol. 3, 21-28 (1996).
9. Uppu, D. S. S. M. et al. Polymers with tunable side-chain amphiphilicity as nonhemolytic antibacterial agents. Chem. Commun. 49, 9389-9391 (2013).
10. Ghosh, C. et al. Small molecular antibacterial peptoid mimics: the simpler the better!. J. Med. Chem. 57, 1428-1436 (2014).
11. Hu, Y. et al. Lipidated peptidomimetics with improved antimicrobial activity. ACS Med. Chem. Lett. 3, 683-686 (2012).
12. Choi, S. et al. De novo design and in vivo activity of conformationally restrained antimicrobial arylamide foldamers. Proc. Natl Acad. Sci. USA 106, 6968-6973 (2009).
13. Lai, X. Z. et al. Ceragenins: cholic acid-based mimics of antimicrobial peptides. Acc. Chem. Res. 41, 1233-1240 (2008).
14. Moraski, G. C., Thanassi, J. A., Podos, S. D., Pucci, M. J., Miller, M. J. One step syntheses of nitrofuranyl benzimidazoles that are active against multi-drug resistant bacteria. J. Antibiot. 64, 667-671 (2011).
15. O'Daniel, P. I. et al. Discovery of a new class of non-β-lactam inhibitors of penicillinbinding proteins with Gram-positive antibacterial activity. J. Am. Chem. Soc. 136, 3664-3672 (2014).
16. Nguyen, K. T. et al. Genetically engineered lipopeptide antibiotics related to A54145 and daptomycin with improved properties. Antimicrob. Agents Chemother. 54, 1404-1413 (2010).
17. Ashford, P. A., Bew, S. P. Recent advances in the synthesis of new glycopeptide antibiotics. Chem. Soc. Rev. 41, 957-978 (2012).
18. Yoshida, O. et al. Novel semi-synthetic glycopeptide antibiotics active against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci (VRE): doubly modified water-soluble derivatives of chloroorienticin B. Bioorg. Med. Chem. Lett. 12, 3027-3031 (2002).
19. Nakama, Y. et al. Discovery of a novel series of semisynthetic vancomycin derivatives effective against vancomycin-resistant bacteria. J. Med. Chem. 53, 2528-2533 (2010).
20. Mu, Y. Q., Nodwell, M., Pace, J. L., Shaw, J. P., Judice, J. K. Vancomycin disulfide derivatives as antibacterial agents. Bioorg. Med. Chem. Lett. 14, 735-738 (2004).
21. Chen, L. et al. Vancomycin analogues active against vanA-resistant strains inhibit bacterial transglycosylase without binding substrate. Proc. Natl Acad. Sci. USA 100, 5658-5663 (2003).
22. Blizzard, T. A. et al. Antibacterial activity of G6-quaternary ammonium derivatives of a lipophilic vancomycin analogue. Bioorg. Med. Chem. Lett. 12, 849-852 (2002).
23. Nagarajan, R., Schabel, A. A., Occolowitz, J. L., Counter, F. T. Synthesis and antibacterial evaluation of N-alkyl vancomycins. J. Antibiot. 41, 63-72 (1989).
24. Griffith, B. R. et al. Model for antibiotic optimization via neoglycosylation: synthesis of liponeoglycopeptides active against VRE. J. Am. Chem. Soc. 129, 8150-8155 (2007).
25. Peltier-Pain, P., Marchillo, K., Andes, D. R., Thorson, J. S. Natural product disaccharide engineering through tandem glycosyltransferase catalysis reversibility and neoglycosylation. Org. Lett. 14, 5086-5089 (2012).
26. Arimato, H., Nishimura, K., Kinumi, T., Hayakawa, I., Uemura, D. Multivalent polymer of vancomycin: enhanced antibacterial activity against VRE. Chem. Commun. 15, 1361-1362 (1999).
27. Pavlov, A. Y., Miroshnikova, O. V., Printsevskaya, S. S., Olsufyeva, E. N., Preobrazhenskaya, M. N. Synthesis of hydrophobic N'-mono and N', N-double alkylated eremomycins inhibiting the transglycosylation stage of bacterial cell wall biosynthesis. J. Antibiot. 54, 455-459 (2001).
28. Maffioli, S. I. et al. Synthesis and antibacterial activity of alkyl derivatives of the glycopeptide antibiotic A40926 and their amides. Bioorg. Med. Chem. Lett. 15, 3801-3805 (2005).
29. Haldar, J., Yarlagadda, V., Akkapeddi, P. Cationic antibacterial composition. WO Patent 072838 (2013).
30. Yarlagadda, V., Akkapeddi, P., Manjunath, G. B., Haldar, J. Membrane active vancomycin analogues: a novel strategy to combat bacterial resistance. J. Med. Chem. 57, 4558-4568 (2014).
31. Zhanel, G. G. et al. New lipoglycopeptides: a comparative review of dalbavancin, oritavancin and telavancin. Drugs 70, 859-886 (2010).
32. James, R. C., Pierce, J. G., Okano, A., Xie, J., Boger, D. L. Redesign of glycopeptide antibiotics: back to the future. ACS Chem. Biol. 7, 797-804 (2012).
33. Xie, J., Pierce, J. G., James, R. C., Okano, A., Boger, D. L. A redesigned vancomycin engineered for dual D-Ala-D-Ala and D-Ala-D-Lac binding exhibits potent antimicrobial activity against vancomycin-resistant bacteria. J. Am. Chem. Soc. 133, 13946-13949 (2011).
34. Nitanai, Y. et al. Crystal structures of the complexes between vancomycin and cell-wall precursor analogs. J. Mol. Biol. 385, 1422-1432 (2009).
35. Fekete, A., Borbas, A., Antus, S., Liptak, A. Synthesis of 3, 6-branched arabinogalactantype tetra- and hexasaccharides for characterization of monoclonal antibodies. Carbohydr. Res. 344, 1434-1441 (2009).
36. Blanzat, M. et al. New catanionic glycolipids. 1. Synthesis, characterization, and biological activity of double-chain and gemini cationic analogues of galactosylceramide (galβ1cer). Langmuir 15, 6163-6169 (1999).
37. Thayer, D. A., Wong, C. H. Vancomycin analogues containing monosaccharides exhibit improved antibiotic activity: a combined one-pot enzymatic glycosylation and chemical diversification strategy. Chem. Asian J. 1, 445-452 (2006).
38. Sundram, U. N., Griffin, J. H. General and efficient method for the solution and solid phase synthesis of vancomycin carboxamide derivatives. J. Org. Chem. 60, 1102-1103 (1995).
39. Wiegand, I., Hilpert, K., Hancock, R. E. W. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3, 163-175 (2008).
40. Draghi, D. C. et al. In vitro activity of telavancin against recent Gram-positive clinical isolates: results of the 2004-05 Prospective European Surveillance Initiative. J. Antimicrob. Chemother. 62, 116-121 (2008).
41. Biedenbach, D. J., Bell, J. M., Sader, H. S., Turnidge, J. D., Jones, R. N. Activities of dalbavancin against a worldwide collection of 81 673 Gram-positive bacterial isolates. Antimicrob. Agents Chemother. 53, 1260-1263 (2009).
42. Perkins, H. R. Specificity of combination between mucopeptide precursors and vancomycin or ristocetin. Biochem. J. 111, 195-205 (1969).
43. Nieto, M., Perkins, H. R. Physicochemical properties of vancomycin and iodovancomycin and their complexes with diacetyl L-lysyl-D-alanyl-D-alanine. Biochem. J. 123, 773-787 (1971).
44. Crowley, B. M., Boger, D. L. Total synthesis and evaluation of [ψ(CH2NH)Tpg4] vancomycin aglycon: reengineering vancomycin for dual D-Ala-D-Ala and D-Ala-D-Lac binding. J. Am. Chem. Soc. 128, 2885-2892 (2006).
45. Slusarz, R., Szulc, M., Madaj, J. Molecular modeling of Gram-positive bacteria peptidoglycan layer, selected glycopeptide antibiotics and vancomycin derivatives modified with sugar moieties. Carbohydr. Res 389, 154-164 (2014).
46. Allen, N. E., Nicas, T. I. Mechanism of action of oritavancin and related glycopeptide antibiotics. FEMS Microbiol. Rev. 26, 511-532 (2003).
47. Ge, M. et al. Vancomycin derivatives that inhibit peptidoglycan biosynthesis without binding D-Ala-D-Ala. Science 284, 507-511 (1999).
48. Eggert, U. S. et al. Genetic basis for activity difference between vancomycin and glycolipid derivatives of vancomycin. Science 294, 361-364 (2001).
49. Higgins, D. L. et al. Telavancin, a multifunctional lipoglycopeptide, disrupts both cell wall synthesis and cell membrane integrity in methicillinresistant Staphylococcus aureus. Antimicrob. Agents Chemother. 49, 1127-1134 (2005).
50. Domenech, O. et al. Interactions of oritavancin, a new lipoglycopeptide derived from vancomycin, with phospholipid bilayers: effect on membrane permeability and nanoscale lipid membrane organization. Biochim. Biophys. Acta 1788, 1832-1840 (2009).
51. Allen, N. E., LeTourneau, D. L., Hobbs, J. N. Jr. The role of hydrophobic side chains as determinants of antibacterial activity of semisynthetic glycopeptide antibiotics. J. Antibiot. 50, 677-684 (1997).
52. Kim, S. J., Tanaka, K. S., Dietrich, E., Rafai Far, A., Schaefer, J. Locations of the hydrophobic side chains of lipoglycopeptides bound to the peptidoglycan of Staphylococcus aureus. Biochemistry 52, 3405-3414 (2013).