Squalamine as an example of a new potent antimicrobial agents class: A critical review

Current Medicinal Chemistry

Volumn 17, Issue 32, 2010, Pages 3909-3917

  Alhanout, K ^a   Rolain, J M ^a   Brunel, J M ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Aminosterol; Antimicrobial agents; Mechanism of action; Squalamine

Indexed keywords

AMINOSTEROL; ANTIINFECTIVE AGENT; CERAGENIN 2; CERAGENIN 3; CERAGENIN 4; CHLOROQUINE; COLISTIN; ERYTHROMYCIN; PUTRESCINE; RIFAMPICIN; SPERMINE; SQUALAMINE; UNCLASSIFIED DRUG;

ACHROMOBACTER XYLOSOXIDANS; ACINETOBACTER BAUMANNII; ANTIBIOTIC RESISTANCE; ANTIMALARIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; ASPERGILLUS FUMIGATUS; BACTERIAL MEMBRANE; BURKHOLDERIA CEPACIA; CANDIDA ALBICANS; DRUG MECHANISM; DRUG POTENTIATION; DRUG STRUCTURE; ENTEROBACTER AEROGENES; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FUSARIUM; HAEMOPHILUS INFLUENZAE; HUMAN; KLEBSIELLA PNEUMONIAE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROSTATE CANCER; PSEUDOMONAS AERUGINOSA; RETINA MACULA AGE RELATED DEGENERATION; RHIZOPUS; SALMONELLA TYPHIMURIUM; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES; STRUCTURE ACTIVITY RELATION; UNSPECIFIED SIDE EFFECT;

ANTI-INFECTIVE AGENTS; BACTERIA; CHOLESTANOLS;

EID: 78650674099     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986710793205417     Document Type: Article

References (53)

1. Kaier, K.; Wilson, C.; Chalkley, M.; Davey, P. G.; Suetens, C.; Grundmann, H.; de, Kraker. M.; Schumacher, M.; Wolkewitz, M.; Frank, U. Health and economic impacts of antibiotic resistance in European hospitals-outlook on the BURDEN project. Infection 2008, 36(5), 492-494.
2. Tacconelli, E. Antimicrobial use: risk driver of multidrug resistant microorganisms in healthcare settings. Curr. Opin. Infect. Dis. 2009, 22(4), 352-358.
3. Salmi, C.; Brunel, J. M. Therapeutic potential of cationic steroid antibacterials. Expert. Opin. Investig. Drugs 2007, 16(8), 1143-1157.
4. Savage, P. B.; Li, C.; Taotafa, U.; Ding, B.; Guan, Q. Antibacterial properties of cationic steroid antibiotics. FEMS Microbiol. Lett. 2002, 217(1), 1-7.
5. Savage, P. B.; Li, C. Cholic acid derivatives: novel antimicrobials. Expert. Opin. Investig. Drugs 2000, 9(2), 263-272.
6. Hao, D.; Hammond, L. A.; Eckhardt, S. G.; Patnaik, A.; Takimoto, C. H.; Schwartz, G. H.; Goetz, A. D.; Tolcher, A. W.; McCreery, H. A.; Mamun, K.; Williams, J. I.; Holroyd, K. J.; Rowinsky, E. K. A Phase I and pharmacokinetic study of squalamine, an aminosterol angiogenesis inhibitor. Clin. Cancer Res. 2003, 9(7), 2465-2471.
7. Herbst, R. S.; Hammond, L. A.; Carbone, D. P.; Tran, H. T.; Holroyd, K. J.; Desai, A.; Williams, J. I.; Bekele, B. N.; Hait, H.; Allgood, V.; Solomon, S.; Schiller, J. H. A phase I/IIA trial of continuous fiveday infusion of squalamine lactate (MSI-1256F) plus carboplatin and paclitaxel in patients with advanced non-small cell lung cancer. Clin. Cancer Res. 2003, 9(11), 4108-4115.
8. Li, D.; Williams, J. I.; Pietras, R. J. Squalamine and cisplatin block angiogenesis and growth of human ovarian cancer cells with or without HER-2 gene overexpression. Oncogene 2002, 21(18), 2805-2814.
9. Sills, A. K., Jr.; Williams, J. I.; Tyler, B. M.; Epstein, D. S.; Sipos, E. P.; Davis, J. D.; McLane, M. P.; Pitchford, S.; Cheshire, K.; Gannon, F. H.; Kinney, W. A.; Chao, T. L.; Donowitz, M.; Laterra, J.; Zasloff, M.; Brem, H. Squalamine inhibits angiogenesis and solid tumor growth in vivo and perturbs embryonic vasculature. Cancer Res. 1998, 58(13), 2784-2792.
10. Teicher, B. A.; Williams, J. I.; Takeuchi, H.; Ara, G.; Herbst, R. S.; Buxton, D. Potential of the aminosterol, squalamine in combination therapy in the rat 13, 762 mammary carcinoma and the murine Lewis lung carcinoma. Anticancer Res. 1998, 18 (4 A), 2567-2573.
11. Chernova, M. N.; Vandorpe, D. H.; Clark, J. S.; Williams, J. I.; Zasloff, M. A.; Jiang, L.; Alper, S. L. Apparent receptor-mediated activation of Ca2+-dependent conductive Cl-transport by sharkderived polyaminosterols. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289(6), R1644-R1658.
12. Ahima, R. S.; Patel, H. R.; Takahashi, N.; Qi, Y.; Hileman, S. M.; Zasloff, M. A. Appetite suppression and weight reduction by a centrally active aminosterol. Diabetes 2002, 51(7), 2099-2104.
13. Higgins, R. D.; Yan, Y.; Geng, Y.; Zasloff, M.; Williams, J. I. Regression of retinopathy by squalamine in a mouse model. Pediatr. Res. 2004, 56(1), 144-149.
14. Higgins, R. D.; Sanders, R. J.; Yan, Y.; Zasloff, M.; Williams, J. I. Squalamine improves retinal neovascularization. Invest. Ophthalmol. Vis. Sci. 2000, 41(6), 1507-1512.
15. Zasloff, M.; Williams, J. I.; Chen, Q.; Anderson, M.; Maeder, T.; Holroyd, K.; Jones, S.; Kinney, W.; Cheshire, K.; McLane, M. A. spermine-coupled cholesterol metabolite from the shark with potent appetite suppressant and antidiabetic properties. Int. J. Obes. Relat. Metab. Disord. 2001, 25(5), 689-697.
16. Brunel, J. M.; Salmi, C.; Loncle, C.; Vidal, N.; Letourneux, Y. Squalamine: a polyvalent drug of the future? Curr. Cancer Drug Targets 2005, 5(4), 267-272.
17. Rao, M. N.; Shinnar, A. E.; Noecker, L. A.; Chao, T. L.; Feibush, B.; Snyder, B.; Sharkansky, I.; Sarkahian, A.; Zhang, X.; Jones, S. R.; Kinney, W. A.; Zasloff, M. Aminosterols from the dogfish shark Squalus acanthias. J. Natl. Prod. 2000, 63(5), 631-635.
18. Senior, K. New aminosterols from the dogfish shark. Drug Discov. Today 2000, 5(7), 267-268.
19. Moore, K. S.; Wehrli, S.; Roder, H.; Rogers, M.; Forrest, J. N., Jr.; McCrimmon, D.; Zasloff, M. Squalamine: an aminosterol antibiotic from the shark. Proc. Natl. Acad. Sci. U. S. A. 1993, 90(4), 1354-1358.
20. Wehrli, S. L.; Moore, K. S.; Roder, H.; Durell, S.; Zasloff, M. Structure of the novel steroidal antibiotic squalamine determined by two-dimensional NMR spectroscopy. Steroids 1993, 58(8), 370-378.
21. Brunel, J. M.; Letourneux, Y. Recent Advances in the Synthesis of Spermine and Spermidine Analogs of the Shark Aminosterol Squalamine. Eur. J. Org. Chem. 2003, (20), 3897-3907.
22. Chen, W. H.; Shao, X. B.; Moellering, R.; Wennersten, C.; Regen, S. L. A bioconjugate approach toward squalamine mimics: Insight into the mechanism of biological action. Bioconjug. Chem. 2006, 17(6), 1582-1591.
23. Choucair, B.; Dherbomez, M.; Roussakis, C.; El-kihel, L. Synthesis of 7 alpha-and 7 beta-spermidinylcholesterol, squalamine analogues. Bioorg. Med. Chem. Lett. 2004, 14(16), 4213-4216. (Pubitemid 38916937)
24. Jones, S. R.; Kinney, W. A.; Zhang, X.; Jones, L. M.; Selinsky, B. S. The synthesis and characterization of analogs of the antimicrobial compound squalamine: 6 beta-hydroxy-3-aminosterols synthesized from hyodeoxycholic acid. Steroids 1996, 61(10), 565-571.
25. Kim, H. S.; Choi, B. S.; Kwon, K. C.; Lee, S. O.; Kwak, H. J.; Lee, C. H. Synthesis and antimicrobial activity of squalamine analogue. Bioorg. Med. Chem. 2000, 8(8), 2059-2065.
26. Shu, Y.; Jones, S. R.; Kinney, W. A.; Selinsky, B. S. The synthesis of spermine analogs of the shark aminosterol squalamine. Steroids 2002, 67 (3-4), 291-304.
27. Salmi, C.; Loncle, C.; Vidal, N.; Laget, M.; Letourneux, Y.; Brunel, J. M. Antimicrobial activities of 3-amino-and polyaminosterol analogues of squalamine and trodusquemine. J. Enzyme Inhib. Med. Chem. 2008, 23(6), 860-865.
28. Salmi, C.; Loncle, C.; Vidal, N.; Letourneux, Y.; Brunel, J. M. New stereoselective titanium reductive amination synthesis of 3-amino and polyaminosterol derivatives possessing antimicrobial activities. Eur. J. Med. Chem. 2008, 43(3), 540-547.
29. Kikuchi, K.; Bernard, E. M.; Sadownik, A.; Regen, S. L.; Armstrong, D. Antimicrobial activities of squalamine mimics. Antimicrob. Agents Chemother. 1997, 41(7), 1433-1438.
30. Salmi, C.; Loncle, C.; Vidal, N.; Letourneux, Y.; Fantini, J.; Maresca, M.; Taieb, N.; Pages, J. M.; Brunel, J. M. Squalamine: an appropriate strategy against the emergence of multidrug resistant gram-negative bacteria? PLoS ONE 2008, 3(7), e2765.
31. Lai, X. Z.; Feng, Y.; Pollard, J.; Chin, J. N.; Rybak, M. J.; Bucki, R.; Epand, R. F.; Epand, R. M.; Savage, P. B. Ceragenins: cholic acidbased mimics of antimicrobial peptides. Acc. Chem. Res. 2008, 41(10), 1233-1240.
32. Ding, B.; Guan, Q.; Walsh, J. P.; Boswell, J. S.; Winter, T. W.; Winter, E. S.; Boyd, S. S.; Li, C.; Savage, P. B. Correlation of the antibacterial activities of cationic peptide antibiotics and cationic steroid antibiotics. J. Med. Chem. 2002, 45(3), 663-669.
33. Epand, R. M.; Epand, R. F.; Savage, P. B. Ceragenins (cationic steroid compounds), a novel class of antimicrobial agents. Drug News Perspect. 2008, 21(6), 307-311.
34. Chin, J. N.; Rybak, M. J.; Cheung, C. M.; Savage, P. B. Antimicrobial activities of ceragenins against clinical isolates of resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 2007, 51(4), 1268-1273.
35. Chin, J. N.; Jones, R. N.; Sader, H. S.; Savage, P. B.; Rybak, M. J. Potential synergy activity of the novel ceragenin, CSA-13, against clinical isolates of Pseudomonas aeruginosa, including multidrugresistant P. aeruginosa. J. Antimicrob. Chemother. 2008, 61(2), 365-370.
36. Schmidt, E. J.; Boswell, J. S.; Walsh, J. P.; Schellenberg, M. M.; Winter, T. W.; Li, C.; Allman, G. W.; Savage, P. B. Activities of cholic acid-derived antimicrobial agents against multidrug-resistant bacteria. J. Antimicrob. Chemother. 2001, 47(5), 671-674.
37. Alhanout, K.; Brunel, J. M.; Raoult, D.; Rolain, J. M. In vitro antibacterial activity of aminosterols against multidrug-resistant bacteria from patients with cystic fibrosis. J Antimicrob Chemother 2009, 64(4), 810-814.
38. Pritt, B.; O'Brien, L.; Winn, W. Mucoid Pseudomonas in cystic fibrosis. Am. J. Clin. Pathol. 2007, 128(1), 32-34.
39. Llobet, E.; Tomas, J. M.; Bengoechea, J. A. Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 2008, 154 (Pt 12), 3877-3886.
40. Zavascki, A. P.; Goldani, L. Z.; Li, J.; Nation, R. L. Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J. Antimicrob. Chemother. 2007, 60(6), 1206-1215.
41. Alhanout, K.; Malesinki, S.; Vidal, N.; Peyrot, V.; Rolain, J. M.; Brunel, J. M. New insights on the antibacterial mechanism of action of squalamine. J. Antimicrob. Chemother. 2010, 65(8), 1688-1693.
42. Selinsky, B. S.; Zhou, Z.; Fojtik, K. G.; Jones, S. R.; Dollahon, N. R.; Shinnar, A. E. The aminosterol antibiotic squalamine permeabilizes large unilamellar phospholipid vesicles. Biochim. Biophys. Acta 1998, 1370(2), 218-234.
43. Saha, S.; Savage, P. B.; Bal, M. Enhancement of the efficacy of erythromycin in multiple antibiotic-resistant gram-negative bacterial pathogens. J. Appl. Microbiol. 2008, 105(3), 822-828.
44. Ding, B.; Yin, N.; Liu, Y.; Cardenas-Garcia, J.; Evanson, R.; Orsak, T.; Fan, M.; Turin, G.; Savage, P. B. Origins of cell selectivity of cationic steroid antibiotics. J. Am. Chem. Soc. 2004, 126(42), 13642-13648.
45. Li, J.; Nation, R. L.; Milne, R. W.; Turnidge, J. D.; Coulthard, K. Evaluation of colistin as an agent against multi-resistant Gramnegative bacteria. Int. J. Antimicrob. Agents 2005, 25(1), 11-25.
46. Jenssen, H.; Hamill, P.; Hancock, R. E. Peptide antimicrobial agents. Clin. Microbiol. Rev. 2006, 19(3), 491-511.
47. Di Pasquale E.; Salmi-Smail, C.; Brunel, J. M.; Sanchez, P.; Fantini, J.; Maresca, M. Biophysical studies of the interaction of squalamine and other cationic amphiphilic molecules with bacterial and eukaryotic membranes: importance of the distribution coefficient in membrane selectivity. Chem. Phys. Lipids 2010, 163(2), 131-140.
48. Alhanout, K.; Djouhri, L.; Vidal, N.; Brunel, J. M.; Piarroux, R.; Ranque, S. In Vitro activity of aminosterols against yeasts isolated from blood stream infections. Med. Mycol. 2010, [Epub ahead of print].
49. Alhanout, K.; Brunel, J. M.; Ranque, S.; Rolain, J. M. In vitro antifungal activity of aminosterols against moulds isolated from cystic fibrosis patients. J. Antimicrob. Chemother. 2010, 65(6), 1307-1309.
50. Salmi, C.; Loncle, C.; Vidal, N.; Rogier, C.; Letourneux, Y.; Pradines, B.; Brunel, J. M. 3-Aminosterol Compounds as a New Class of Anti-Malarial Agents against Chloroquine-Susceptible and - Resistant Plasmodium falciparum. Lett. Drug Design Discov. 2008, 6(2), 163-166.
51. Leszczynska, K.; Namiot, A.; Fein, D. E.; Wen, Q.; Namiot, Z.; Savage, P. B.; Diamond, S.; Janmey, P. A.; Bucki, R. Bactericidal activities of the cationic steroid CSA-13 and the cathelicidin peptide LL-37 against Helicobacter pylori in simulated gastric juice. BMC Microbiol. 2009, 9, 187.
52. Lavigne, J. P.; Brunel, J. M.; Chevalier, J.; Pages J. M. Squalamine, an original chemosensitizer to combat antibiotic-resistant Gramnegative bacteria. J. Antimicrob. Chemother. 2010, 65(4), 799-801.
53. Singh, S. S. Preclinical pharmacokinetics: an approach towards safer and efficacious drugs. Curr. Drug Metab. 2006, 7(2), 165-182.