Next generation biofilm inhibitors for Pseudomonas aeruginosa: Synthesis and rational design approaches

Current Topics in Medicinal Chemistry

Volumn 14, Issue 1, 2014, Pages 81-109

  Majik, Mahesh S ^a   Parvatkar, Prakash T ^a  

^a NATIONAL INSTITUTE OF OCEANOGRAPHY   (India)

Author keywords

Antifouling; Biofilms; Chemical signaling; Marine natural products; Quorum sensing inhibitors

Indexed keywords

ALGINATE LYASE; AMINO IMIDAZOLE DERIVATIVE; ANTIINFECTIVE AGENT; AZITHROMYCIN; BROMINATED FURANONE DERIVATIVE; FERRIC AMMONIUM CITRATE; FURANONE DERIVATIVE; GALLIUM; GARLIC EXTRACT; HYDROGEN PEROXIDE; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; LACTOFERRIN; LYASE; N ACYLHOMOSERINE LACTONE; ORGANOSULFUR DERIVATIVE; PENICILLIN DERIVATIVE; PYRROLIDINE DERIVATIVE; TOBRAMYCIN; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

AGONIST; ANTIBIOFILM ACTIVITY; APOPTOSIS; BACTERIAL BIOFILM; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL VIRULENCE; DOSE RESPONSE; DRUG ACTIVITY; DRUG ANTAGONISM; DRUG DESIGN; DRUG SYNTHESIS; HOSPITAL INFECTION; HUMAN; IC 50; NONHUMAN; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION;

4-BUTYROLACTONE; ANTI-BACTERIAL AGENTS; AQUATIC ORGANISMS; BIOFILMS; DRUG DESIGN; HUMANS; INDOLES; PSEUDOMONAS AERUGINOSA; SULFUR COMPOUNDS;

EID: 84891788019     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026613666131113152257     Document Type: Review

References (86)

1. Davies, D.G.; Parsek, M.R.; Pearson, J.P.; Iglewski, B.H.; Costerton, J.W.; Greenberg, E.P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 1998, 280, 295-298.
2. Stewart, P.S. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol., 2002, 292, 107-113.
3. Del Pozo, J.L.; Patel, R. The challenge of treating biofilmassociated bacterial infections. Clin Pharmacol. Ther., 2007, 82, 204-209.
4. Worthington, R.J.; Richards, J.J.; Melander C. Small molecule control bacterial biofilms. Org. Biomol. Chem., 2012, 10, 7457-7474.
5. Fuqua, W.C.; Winans, S.C.; Greenberg, E.P. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol., 1994, 176, 269-275.
6. Henke, J.M.; Bassler, B.L. Bacterial social engagements. Trends Cell Biol., 2004, 14, 648-656.
7. Pearson, J.P.; Gray, K.M.; Passador, L. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Science USA, 1994, 91, 197-201.
8. Gambello, M.J.; Iglewski, B.H. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J. Bacteriol, 1991, 173, 3000-3009.
9. Pearson, J.P.; Pesci, E.C. Iglewski, B.H. Roles of Pseudomonas aeruginosa las and rhl Quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol., 1997, 179, 5756-5767.
10. Wu, H.; Song, Z.; Hentzer, M. Detection of N-acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa. Microbiol., 2000, 146, 2481-2493,
11. Middleton B.; Rodgers HC, Camara M. Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol. Lett., 2002, 207, 1-7.
12. Deziel, E.; Lepine, F.; Milot, S. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA, 2004, 101, 1339-1344;
13. Diggle, S.P.; Matthijs, S.; Wright, V.J. The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem. Biol., 2007, 14, 87-96.
14. Hakenbeck, R.; Stock, J.B. Analysis of two-component signal transduction systems involved in transcriptional regulation. Methods Enzymol., 1996, 273, 281-300.
15. Ohnishi, Y.; Kameyama, S.; Onaka, H.; Horinouchi, S. The Afactor regulatory cascade leading to streptomycin biosynthesis in Streptomyces griseus: identification of a target gene of the Afactor receptor. Mol. Mircobiol., 1999, 34, 102-111.
16. Bassler, B.L.; Wright, M.; Silverman, M.R. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol., 1994, 13, 273-286.
17. Chen, X.; Schauder, S.; Potier, N.; Van Dorsselaer, A.; Pelczer, I.; Bassler, B.L.; Hughson, F.M. Structural identification of a bacterial quorum-sensing signal containing boron. Nature, 2002, 415, 545-549.
18. Rader, B.A.; Campagna, S.R.; Semmelhack, M.F. The quorumsensing molecule autoinducer 2 regulates motility and flagellar morphogenesis in Helicobacter pylori. J. Bacteriol., 2007, 189, 6109-6117.
19. He, Y.W.; Xu, M.; Lin, K.; Alvin Ng, J-Y.; Wen, C-M.; Wang. LH.; Liu, Z-D.; Zhang, H-B.; Dong, Y-H.; Maxwell Dow, J.; Zhang, L-H. Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell-cell communication-dependent genes and functions. Mol. Microbiol., 2006, 59, 610-622.
20. Nickerson, K.W.; Atkin, A.L.; Hornby, J.M. Quorum sensing in dimorphic fungi: farnesol and beyond. Appl. Environ. Microbiol., 2006, 72, 3805-3813.
21. Williams, P., Camara, M., Hardman, A.; Swift, S.; Milton, D.; Hope, V.J.; Winzer, K.; Middleton, B.; Pritchard, D.I.; Bycroft, B.W. Quorum sensing and the population-dependent control of virulence. Philos. Trans. R Soc. Lond. B Biol Sci., 2000, 355, 667-680.
22. Costerton, J.W.; Stewart, P.S.; Greenberg, E.P. Bacterial biofilms: a common cause of persistent infections. Science, 1999, 284, 1318-1322.
23. Clatworthy, A.E.; Pierson, E.; Hung, D.T. Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol., 2007, 3, 541-548.
24. Martinez, J.L.; Baquero, F. Mutation frequencies and antibiotic resistance. Antimicrob. Agents Chemother., 2000, 44, 1771-1777.
25. Feldman, M.; Bryan, R.; Rajan, S.; Scheffler, L.; Brunnert, S.; Tang, H.; Prince, A. Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun., 1998, 66, 43-51.
26. Costerton, J.W.; Stewart, P.S.; Greenberg, E.P. Bacterial biofilms: a common cause of persistent infections. Science, 1999, 284, 1318-1322.
27. Alkawash, M.A.; Soothill, J.S.; Schiller, N.L. Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. Apmis, 2006, 114, 131-138.
28. Hoffmann, N.; Lee, B.; Hentzer, M.; Rasmussen, T.B.; Song, Z.; Johansen, H.K.; Givskov, M.; Hoiby, N. Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr (-/-) mice. Antimicrob. Agents Chemother., 2007, 51, 3677-3687.
29. Singh, P.K.; Parsek, M.R.; Greenberg, E.P.; Welsh, M.J. A component of innate immunity prevents bacterial biofilm development. Nature, 2002, 417, 552-555.
30. Kaneko, Y.; Thoendel, M.; Olakanmi, O.; Britigan, B.E.; Singh, P.K. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial & antibiofilm activity. J. Clin. Invest., 2007, 117, 877-888.
31. Musk, D.J.; Banko, D.A.; Hergenrother, P.J. Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa. Chem. Biol., 2005, 12, 789-796.
32. Bjarnsholt, T.; Jensen, P.O.; Burmolle, M.; Hentzer, M.; Haagensen, J.A.; Hougen, H.P.; Calum, H.; Madsen, K.G.; Moser, C.; Molin, S.; Hoiby, N.; Givskov, M. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology, 2005, 151, 373-383.
33. Passador, L.; Cook, J.M.; Gambello, M.J.; Rust, L.; Iglewski, B.H. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science, 1993, 260, 1127-1130.
34. Hentzer, M.; Riedel, K.; Rasmussen, T.B.; Heydorn, A.; Andersen, J.B.; Parsek, M.R.; Rice, S.A.; Eberl, L.; Molin, S.; Hoiby, N.; Kjelleberg, S.; Givskov, M. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiol., 2002, 148, 87-102.
35. Manefield, M.; Welch, M.; Givskov, M.; Salmond, G.P.; Kjelleberg, S. Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiol. Lett., 2001, 205, 131-138.
36. Ren, D.; Sims, J.J.; Wood, T.K. Inhibition of biofilm formation and swarming of Bacillus subtilis by (5Z)-4-bromo-5 (bromomethylene)-3-butyl-2 (5H)-furanone. Lett. Appl. Microbiol., 2002, 34, 293-299.
37. Ren, D.C.; Sims, J.J.; Wood, T.K. Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2 (5H)-furanone. Environ. Microbiol., 2001, 3, 731-736.
38. Denys, R.; Wright, A.D.; Konig, G.M.; Sticher, O. Tetrahedron, 1993, 49, 11213-11220.
39. Estephane, J.; Dauvergne, J.; Soulere, L.; Reverchon. S.; Queneau. Y.; Doutheau, A. N-Acyl-3-amino-5H-furanone derivatives as new inhibitors of LuxR-dependent quorum sensing: Synthesis, biological evaluation and binding mode study. Bioorg. Med. Chem. Lett., 2008, 18, 4321-4324.
40. Sabbah, M.; Bernollin, M.; Doutheau, A.; Soulere, L.; Queneau, Y. A new route towards fimbrolide analogues: importance of the exomethylene motif in LuxR dependent quorum sensing inhibition. Med. Chem. Commun., 2013, 4, 363-366.
41. Shetye, G.S.; Singh, N.; Gao, X.; Bandyopadhyay, D.; Yan, A.; Luk, Y.-Y. Structures and biofilm inhibition activities of brominated furanones for Escherichia coli and Pseudomonas aeruginosa. Med. Chem. Commun., 2013, 4, 1079-1084.
42. Hentzer, M.; Riedel, K.; Rasmussen, T.B.; Heydorn, A.; Andersen, J.B.; Parsek, M.R.; Rice, S.A.; Eberl, L.; Molin, S.; Hoiby, N.; Kjelleberg, S.; Givskov, M. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology (Reading, U.K.), 2002, 148, 87-102.
43. Manny, A.J.; Kjelleberg, S.; Kumar, N.; de Nys, R.; Read, R.W.; Steinberg, P. Reinvestigation of the sulfuric acid-catalysed cyclisation of brominated 2-alkyllevulinic acids to 3-alkyl-5-methylene-2 (5H)-furanones. Tetrahedron, 1997, 53, 15813-15826.
44. Han, Y.; Hou, S.; Simon, K.A.; Ren, D.; Luk, Y.-Y. Identifying the important structural elements of brominated furanones for inhibiting biofilm formation by Escherichia coli. Bioorg. Med. Chem. Lett., 2008, 18, 1006-1010.
45. Iskander, G.; Zhang, R.; Chan, D.S.-H.; Black, D.S.; Alamgir, M.; Kumar, N. An efficient synthesis of brominated 4-alkyl-2 (5H)-furanones. Tetrahedron Lett., 2009, 50, 4613-4615.
46. Hjelmgaard, T.; Persson, T.; Rasmussen, T.B.; Givskov, M.; Nielsen, J. Synthesis of furanone-based natural product analogues with quorum sensing antagonist activity. Bioorg. Med. Chem., 2003, 11, 3261-3271.
47. Horikawa, M.; Tateda, K.; Tuzuki, E.; Ishii, Y.; Ueda, C.; Takabatake, T.; Miyairi, S.; Yamaguchi, K.; Ishiguro, M. Synthesis of Pseudomonas quorum-sensing autoinducer analogs and structural entities required for induction of apoptosis in macrophages. Bioorg. Med. Chem. Lett., 2006, 16, 2130-2133.
48. Mattmann, M.E.; Geske, G.D.; Worzalla, G.A.; Chandler, J.R.; Sappington, K.J.; Greenberg, E.P.; Blackwell, H.E. Synthetic ligands that activate and inhibit a quorum-sensing regulator in Pseudomonas aeruginosa. Bioorg. Med. Chem. Lett., 2008, 18, 3072-3075.
49. Lee, J.H.; Lequette, Y.; Greenberg, E.P. Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol. Microbiol., 2006, 59, 602-609.
50. Boukraa, M.; Sabbah, M.; Soulere, L.; El Efrit, M.L.; Queneau, Y.; Doutheau, A. AHL-dependent quorum sensing inhibition: Synthesis and biological evaluation of α-(N-alkyl-carboxamide)-γ-butyrolactones and α-(N-alkyl-sulfonamide)-γ-butyrolactones. Bioorg. Med. Chem. Lett., 2011, 21, 6876-6879.
51. Mattmann, M.E.; Shipway, P.M.; Heth, N.J.; Blackwell, H.E. Potent and selective synthetic modulators of a quorum sensing repressor in Pseudomonas aeruginosa identified from secondgeneration libraries of N-acylated L-homoserine lactones. Chem. Bio. Chem., 2011, 12, 942-949.
52. Geske, G.D.; O'Neill, J.C.; Miller, D.M.; Mattmann, R.J.; Blackwell, H.E. Modulation of bacterial quorum sensing with synthetic ligands: A systematic evaluation of N-acylated homoserine lactones in multiple species and new insights into their mechanisms of action. J. Am. Chem. Soc., 2007, 129, 13613-13625.
53. Brackman, G.; Risseeuw, M.; Celen, S.; Cos, P.; Maes, L.; Nelis, H.J.; Calenbergh, V.; Coenye, T. Synthesis and evaluation of the quorum sensing inhibitory effect of substituted triazolyldihydrofuranones. Bioorg. Med. Chem., 2012, 20, 4737-4743.
54. Stacy, D.M.; Le Quement, S.T.; Hansen, C.L.; Clausen, J.W.; Tolker-Nielsen, T.; Brummond, J.W.; Givskov, M.; Nielsen, T.E.; Blackwell, H.E. Synthesis and biological evaluation of triazolecontaining N-acyl homoserine lactones as quorum sensing modulators. Org. Biomol. Chem., 2013, 11, 938-954.
55. Yamada, A.; Kitamura, H.; Yamaguchi, K.; Fukuzawa, S.; Kamijima, C.; Yazawa, K.; Kuramoto, M.; Wang, G.Y.S.; Fujitani, Y.; Uemura, D. Development of chemical substances regulating biofilm formation. Bull. Chem. Soc. Jpn., 1997, 70, 3061-3069.
56. Chanas, B.; Pawlik, J.R.; Lindel, T.; Fenical, W. Chemical defense of the Caribbean sponge Agelas clathrodes. J. Exp. Mar. Biol. Ecol., 1997, 208, 185-196
57. Huigens, R.W.; Richards, J.J.; Parise, G.; Ballard, T.E.; Zeng, W.; Deora, R.; Melander, C. Inhibition of Pseudomonas aeruginosa biofilm formation with bromoageliferin analogues. J. Am. Chem. Soc., 2007, 129, 6966-6967.
58. Nicolaou, K.C.; Liu, J.J.; Yang, Z.; Ueno, H.; Sorensen, E.J.; Claiborne, C.F.; Guy, R.K.; Hwang, C.K.; Nakada, M.; Nantermet, P.G. Total synthesis of taxol. 2. Construction of A and C ring intermediates and initial attempts to construct the ABC ring system. J. Am. Chem. Soc., 1995, 117, 634-644.
59. Ochiai, H.; Ohtani, T.; Ishida, A.; Kishikawa, K.; Yamamoto, S.; Takeda, H.; Obata, T.; Nakai, H.; Toda, M. Orally active PDE4 inhibitor with therapeutic potential. Eur. J. Med. Chem., 2004, 39, 555-571.
60. Olofson, A.; Yakushijin, K.; Horne, D.A. Synthesis of marine sponge alkaloids oroidin, clathrodin, and dispacamides. Preparation and transformation of 2-amino-4, 5-dialkoxy-4, 5-dihydroimidazolines from 2-aminoimidazoles. J. Org. Chem., 1998, 63, 1248-1253.
61. Huigens, R.W.; Ma, L.Y.; Gambino, C.; Moeller, P.D.; Basso, A.; Cavanagh, J.; Wozniak, D.; Melander, C. Control of bacterial biofilms with marine alkaloid derivatives. Mol. BioSyst., 2008, 4, 614-621.
62. Huigens, R.W.; Rogers, S.A.; Steinhauer, A.T.; Melander, C. Inhibition of Acinetobacter baumannii, Staphylococcus aureus and Pseudomonas aeruginosa biofilm formation with a class of TAGEtriazole conjugates. Org. Biomol. Chem., 2009, 7, 794-802.
63. Richards, J.J.; Ballard, T.E.; Huigens, R.W.; Melander, C. Synthesis and screening of an oroidin library against Pseudomonas aeruginosa biofilms. ChemBioChem, 2008, 9, 1267-1279.
64. Bailey, D.M.; Johnson, R.E. Pyrrole antibacterial agents. 2. 4, 5-Dihalopyrrole-2-carboxylic acid derivatives. J. Med. Chem., 1973, 16, 1300-1302.
65. Richards, J.J.; Balllard, T.E.; Melander, C. Inhibition and dispersion of Pseudomonas aeruginosa biofilms with reverse amide 2-aminoimidazole oroidin analogues. Org. Biomol. Chem., 2008, 6, 1356-1363.
66. Li, T.Y.; Hilton, S.; Janda, K.D. The potential application of catalytic antibodies to protecting group removal: Catalytic antibodies with broad substrate tolerance. J. Am. Chem. Soc., 1995, 117, 2123-2127.
67. Roger, S.A.; Melander, C. Construction and screening of a 2-aminoimidazole library identifies a small molecule capable of inhibiting and dispersing bacterial biofilms across order, class and phylum. Angew. Chem. Int. Ed., 2008, 47, 5229-5231.
68. Reed, C.S.; Huigens, R.W.; Rogers, S.A.; Melander, C. Modulating the development of E. coli biofilms with 2-aminoimidazoles. Bioorg. Med. Chem. Lett., 2010, 20, 6310-6312.
69. Furlani, R.E.; Yeagley, A.A.; Melander, C. A flexible approach to 1, 4-disubstituted 2-aminoimidazoles that inhibit and disperse biofilms and potentiate the effects of β-lactams against multi-drug resistant bacteria. Eur. J. Med. Chem., 2013, 62, 59-70.
70. Roger, S.A.; Lindsey, E.A.; Whitehead D.C.; Mullikin, T.; Melander, C. Synthesis and biological evaluation of 2-aminoimidazole/carbamate hybrid anti-biofilm and anti-microbial agents. Bioorg. Med. Chem. Lett., 2011, 21, 1257-1260.
71. Yamada, A.; Kitamura, H.; Yamaguchi, K., Fukuzawa, S.; Kamijima, C.; Yazawa, K.; Kuramoto, M.; Wang, G.Y.S.; Fujitani, Y.; Uemura, D. Development of chemical substances regulating biofilm formation. Bull. Chem. Soc. Jpn., 1997, 70, 3061-3069.
72. Rogers, S.A.; Huigens, R.W.; Melander, C. A 2-aminobenzimidazole that inhibits and disperses Gram-positive biofilms through a zinc-dependent mechanism. J. Am. Chem. Soc., 2009, 131, 9868-9869.
73. Lindsey, E.A.; Brackett, C.M.; Mullikin, T.; Alcarraz, C.; Melander, C. The discovery of N-1-substituted 2-aminobenzimidazoles as zinc-dependent S. aureus biofilm inhibitors. Med. Chem. Commun., 2012, 3, 1462-1465.
74. Bunders, C.A.; Richards, J.J.; Melander, C. Identification of aryl 2-aminoimidazoles as biofilm inhibitors in Gram-negative bacteria. Bioorg. Med. Chem. Lett., 2010, 20, 3797-3800.
75. Richards, J.J.; Melander, C. Synthesis of a 2-Aminoimidazole Library for Antibiofilm Screening Utilizing the Sonogashira Reaction. J. Org. Chem., 2008, 73, 5191-5193.
76. Frei, R.; Breitbach, A.S.; Blackwell, H.E. 2-Aminobenzimidazole derivatives strongly inhibit and disperse Pseudomonas aeruginosa biofilms. Angew. Chem. Int. Ed., 2012, 51, 5226-5229.
77. Block, E. Die Organoschwefelchemie der Gattung Allium und ihre Bedeutung für die organische Chemie des Schwefels. Angew. Chem. Int. ed., 1992, 104, 1158-1203.
78. Persson, T.; Hansen, T.H.; Rasmussen, T.B.; Skinderso, M.E.; Givskov, M.; Nielsen, J. Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org. Biomol. Chem., 2005, 3, 253-262.
79. Cady, N.C.; McKean, K.A.; Behnke, J.; Kubec, R.; Mosier, A.P.; Kasper, S.H.; Burz, D.S.; Musah, R.A. Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural product-inspired organosulfur compounds. PLOS ONE, 2012, 7, 1-12.
80. Benneche, T.; Herstad, G.; Rosenberg, M.; Assev, S.; Scheie, A.A. Facile synthesis of 5-(alkylidene) thiophen-2 (5H)-ones. A new class of antimicrobial agents. RSC Adv., 2011, 1, 323-332.
81. Goh, W.K.; Iskander, G.; Stc Black, D.; Kumar, N. An efficient lactamization of fimbrolides to novel 1, 5-dihydropyrrol-2-ones. Tetrahedron Lett., 2007, 48, 2287-2290.
82. Benneche, T.; Chamgordani, E.J.; Reimer, I. A new synthesis of five-membered heterocyclic quorum sensing inhibitors. Tetrahedron Lett., 2012, 53, 6982-6983.
83. Majik, M.S.; Naik, D.; Bhat, C.; Tilve, S.; Tilvi, S.; D'Souza, L. Synthesis of (R)-norbgugaine and its potential as quorum sensing inhibitor against Pseudomonas aeruginosa. Bioorg. Med. Chem. Lett., 2013, 23, 2353-2356.
84. Malladi, V.L.A.; Sobczak, A.J.; Maricic, N.; Murugapiran, S.K.; Schneper, L.; Makemson, J.; Mathee, K.; Wnuk, S.F. Substituted lactam and cyclic azahemiacetals modulate Pseudomonas aeruginosa quorum sensing. Bioorg. Med. Chem., 2011, 19, 5500-5506.
85. Rogers, S.A.; Whitehead, D.C.; Mullikin T.; Melander, C. Synthesis and bacterial biofilm inhibition studies of ethyl N-(2-phenethyl) carbamate derivatives. Org. Biomol. Chem., 2010, 8, 3857-3859.
86. Ishida, T.; Ikeda, T.; Takiguchi, N.; Kuroda, A.; Ohtake, H.; Kato, J. Inhibition of quorum sensing in Pseudomonas aeruginosa by Nacyl cyclopentylamides. Appl. Environ. Microbiol., 2007, 73, 3183-3188.