Axial hydrogen at C7 position and bumpy tetracyclic core markedly reduce sterol's affinity to amphotericin B in membrane

Biochemistry

Volumn 54, Issue 2, 2015, Pages 303-312

  Nakagawa, Yasuo ^a   Umegawa, Yuichi ^a   Nonomura, Kenichi ^a   Matsushita, Naohiro ^a   Takano, Tetsuro ^a   Tsuchikawa, Hiroshi ^a   Hanashima, Shinya ^a   Oishi, Tohru ^a   Matsumori, Nobuaki ^a   Murata, Michio ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMS; DRUG INTERACTIONS; HYDROGEN; LIPIDS; MAMMALS; METABOLITES; VAN DER WAALS FORCES;

AMPHOTERICIN B; ANTIFUNGAL DRUGS; CONFORMATIONAL ANALYSIS; HYDROGEN ATOMS; INTERMOLECULAR DISTANCE; ROTATIONAL ECHO DOUBLE RESONANCE; SPECTRAL MEASUREMENT; STRUCTURAL DIFFERENCES;

ALCOHOLS;

AMPHOTERICIN B; ERGOSTEROL; HYDROGEN; ANTIFUNGAL AGENT; LIPOSOME; STEROL;

ARTICLE; CHANNEL GATING; COMPLEX FORMATION; FLUORESCENCE; FLUX ASSAY; NUCLEAR MAGNETIC RESONANCE; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; SOLID STATE; STEADY STATE; STEREOSPECIFICITY; STEROL ANALYSIS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CYTOLOGY; DRUG EFFECTS; FUNGUS; HUMAN; METABOLISM; MICROBIOLOGY; MYCOSES;

FUNGI; MAMMALIA;

AMPHOTERICIN B; ANTIFUNGAL AGENTS; CELL MEMBRANE; FUNGI; HUMANS; LIPOSOMES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MYCOSES; STEROLS;

EID: 84922419397     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5012942     Document Type: Article

References (64)

1. Bolard, J. (1986) How do the polyene macrolide antibiotics affect the cellular membrane properties? Biochim. Biophys. Acta 864, 257-304
2. Sugiyama, R., Nishimura, S., Matsumori, N., Tsunematsu, Y., Hattori, A., and Kakeya, H. (2014) Structure and biological activity of 8-deoxyheronamide C from a marine-derived Streptomyces sp.: heronamides target saturated hydrocarbon chains in lipid membranes J. Am. Chem. Soc. 136, 5209-5212
3. Espiritu, R. A., Matsumori, N., Tsuda, M., and Murata, M. (2014) Direct and stereospecific interaction of amphidinol 3 with sterol in lipid bilayers Biochemistry 53, 3287-3293
4. Houdai, T., Matsuoka, S., Matsumori, N., and Murata, M. (2004) Membrane-permeabilizing activities of amphidinol 3, polyene-polyhydroxy antifungal from a marine dinoflagellate Biochim. Biophys. Acta 1667, 91-100
5. Houdai, T., Matsuoka, S., Morsy, N., Matsumori, N., Satake, M., and Murata, M. (2005) Hairpin conformation of amphidinols possibly accounting for potent membrane permeabilizing activities Tetrahedron 61, 2795-2802
6. Morsy, N., Houdai, T., Matsuoka, S., Matsumori, N., Adachi, S., Oishi, T., Murata, M., Iwashita, T., and Fujita, T. (2006) Structures of new amphidinols with truncated polyhydroxyl chain and their membrane-permeabilizing activities Bioorg. Med. Chem. 14, 6548-6554
7. Nishimura, S., Arita, Y., Honda, M., Iwamoto, K., Matsuyama, A., Shirai, A., Kawasaki, H., Kakeya, H., Kobayashi, T., Matsunaga, S., and Yoshida, M. (2010) Marine antifungal theonellamides target 3β-hydroxysterol to activate Rho1 signaling Nat. Chem. Biol. 6, 519-526
8. 2H nuclear magnetic resonance Biochemistry 52, 2410-2418
9. 2H NMR spectroscopy J. Am. Chem. Soc. 131, 11855-11860
10. Ostrosky-Zeichner, L., Marr, K. a, Rex, J. H., and Cohen, S. H. (2003) Amphotericin B: time for a new "gold standard Clin. Infect. Dis. 37, 415-425
11. Lemke, A., Kiderlen, A. F., and Kayser, O. (2005) Amphotericin B Appl. Microbiol. Biotechnol. 68, 151-162
12. Martin, C. A. (2005) Invasive fungal infections in the critically ill patient J. Pharm. Pract. 18, 9-17
13. Duarte, J. M., Betts, R., Rotstein, C., Colombo, A. L., Moya, L. T., Smietana, J., Lupinacci, R., Sable, C., Kartsonis, N., and Perfect, J. (2002) Comparison of caspofungin and amphotericin B for invasive candidiasis N. Engl. J. Med. 347, 2020-2029
14. De Kruijff, B. and Demel, R. A. (1974) Polyene antibiotic-sterol interactions in membranes of acholeplasma laidlawii cells and lecithin liposomes. III. molecular structure of the polyene antibiotic-cholesterol complexes Biochim. Biophys. Acta 339, 57-70
15. Kamiński, D. M. (2014) Recent progress in the study of the interactions of amphotericin B with cholesterol and ergosterol in lipid environments Eur. Biophys. J. 43, 453-467
16. Barwicz, J., Gruda, I., and Tancre, P. (2000) A kinetic study of the oxidation effects of amphotericin B on human low-density lipoproteins FEBS Lett. 465, 83-86
17. Sangalli-Leite, F., Scorzoni, L., Mesa-Arango, A. C., Casas, C., Herrero, E., Gianinni, M. J. S. M., Rodríguez-Tudela, J. L., Cuenca-Estrella, M., and Zaragoza, O. (2011) Amphotericin B mediates killing in Cryptococcus neoformans through the induction of a strong oxidative burst Microbes Infect. 13, 457-467
18. Hartsel, S. and Bolard, J. (1996) Amphotericin B: new life for an old drug Trends Pharmacol. Sci. 17, 445-449
19. Takano, T., Konoki, K., Matsumori, N., and Murata, M. (2009) Amphotericin B-induced ion flux is markedly attenuated in phosphatidylglycerol membrane as evidenced by a newly devised fluorometric method Bioorg. Med. Chem. 17, 6301-6304
20. Anderson, T. M., Clay, M. C., Cioffi, A. G., Diaz, K. a, Hisao, G. S., Tuttle, M. D., Nieuwkoop, A. J., Comellas, G., Maryum, N., Wang, S., Uno, B. E., Wildeman, E. L., Gonen, T., Rienstra, C. M., and Burke, M. D. (2014) Amphotericin forms an extramembranous and fungicidal sterol sponge Nat. Chem. Biol. 10, 400-406
21. Gray, K. C., Palacios, D. S., Dailey, I., Endo, M. M., Uno, B. E., Wilcock, B. C., and Burke, M. D. (2012) Amphotericin primarily kills yeast by simply binding ergosterol Proc. Natl. Acad. Sci. U. S. A. 109, 2234-2239
22. Baginski, M., Czub, J., and Sternal, K. (2006) Interaction of amphotericin B and its selected derivatives with membranes: molecular modeling studies Chem. Rec. 6, 320-332
23. Vertut-Croquin, A., Bolard, J., Chabbert, M., and Gary-Bobo, C. (1983) Differences in the interaction of the polyene antibiotic amphotericin B with cholesterol-or ergosterol-containing phospholipid vesicles. A circular dichroism and permeability study Biochemistry 22, 2939-2944
24. Charbonneau, C., Fournier, I., Dufresne, S., Barwicz, J., and Tancrède, P. (2001) The interactions of amphotericin B with various sterols in relation to its possible use in anticancer therapy Biophys. Chem. 91, 125-133
25. Clejan, S. and Bittman, R. (1985) Rates of amphotericin B and filipin association with Sterols J. Biol. Chem. 260, 2884-2889
26. Chen, W. C. and Bittman, R. (1977) Kinetics of association of amphotericin B with vesicles Biochemistry 16, 4145-4149
27. 31 P-NMR study Biochim. Biophys. Acta 980, 261-272
28. Hsuchen, C. C. and Feingold, D. S. (1973) Selective membrane toxicity of the polyene antibiotics: studies on lecithin membrane models (liposomes) Antimicrob. Agents Chemother. 4, 309-315
29. Matsuoka, S. and Murata, M. (2002) Cholesterol markedly reduces ion permeability induced by membrane-bound amphotericin B Biochim. Biophys. Acta 1564, 429-434
30. Umegawa, Y., Matsumori, N., Oishi, T., and Murata, M. (2008) Ergosterol increases the intermolecular distance of amphotericin B in the membrane-bound assembly as evidenced by solid-state NMR Biochemistry 47, 13463-13469
31. Umegawa, Y., Nakagawa, Y., Tahara, K., Tsuchikawa, H., Matsumori, N., Oishi, T., and Murata, M. (2012) Head-to-tail interaction between amphotericin B and ergosterol occurs in hydrated phospholipid membrane Biochemistry 51, 83-89
32. 31P rotational echo double resonance Biochemistry 44, 704-710
33. Langlet, J., Bergès, J., Caillet, J., and Demaret, J. (1994) Theoretical study of the complexation of amphotericin B with sterols Biochim. Biophys. Acta 1191, 79-93
34. Baginski, M., Resat, H., and Borowski, E. (2002) Comparative molecular dynamics simulations of amphotericin B-cholesterol/ergosterol membrane channels Biochim. Biophys. Acta 1567, 63-78
35. Baran, M., Borowski, E., and Mazerski, J. (2009) Molecular modeling of amphotericin B-ergosterol primary complex in water II Biophys. Chem. 141, 162-168
36. Neumann, A., Czub, J., and Baginski, M. (2009) On the possibility of the amphotericin B-sterol complex formation in cholesterol- and ergosterol-containing lipid bilayers: a molecular dynamics study J. Phys. Chem. B 113, 15875-15885
37. Neumann, A., Baginski, M., and Czub, J. (2010) How do sterols determine the antifungal activity of amphotericin B? Free energy of binding between the drug and its membrane targets J. Am. Chem. Soc. 132, 18266-18272
38. Nakagawa, Y., Umegawa, Y., Takano, T., Tsuchikawa, H., Matsumori, N., and Murata, M. (2014) Effect of sterol side chain on ion channel formation by amphotericin B in lipid bilayers Biochemistry 53, 3088-3094
39. Baginski, M. and Borowski, E. (1997) Distribution of electrostatic potential around amphotericin B and its membrane targets J. Mol. Struct. THEOCHEM 389, 139-146
40. Baginski, M., Bruni, P., and Borowski, E. (1994) Comparative analysis of the distribution of the molecular electrostatic potential for cholesterol and ergosterol J. Mol. Struct. THEOCHEM 311, 285-296
41. Giroux, S. and Corey, E. J. (2008) An efficient, stereocontrolled synthesis of the 25-(R)-diastereomer of dafachronic acid A from beta-ergosterol Org. Lett. 10, 801-802
42. Delseth, C., Kashman, Y., and Djerassi, C. (1979) Ergosta-5,7,9(11),22-tetraen-3β-ol and its 24ξ-ethyl Homolog, two new marine sterols from the red sea sponge biemna fortis Helv. Chim. Acta 62, 2037-2045
43. Ohvo-Rekilä, H., Akerlund, B., and Slotte, J. P. (2000) Cyclodextrin-catalyzed extraction of fluorescent sterols from monolayer membranes and small unilamellar vesicles Chem. Phys. Lipids 105, 167-178
44. 14C] Ergocalcifero J. Chem. Soc., Perkin Trans. 1, 2980-2981
45. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids J. Chem. Phys. 103, 6951-6958
46. Gullion, T., Baker, D., and Conradi, M. (1990) New, compensated carr-purcell sequences J. Magn. Reson. 89, 479-484
47. 80 and flexible docking of 9-deazaguanine inhibitors into PNP J. Comput. Chem. 20, 1671-1684
48. Kaminski, G. and Friesner, R. (2001) Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides J. Phys. Chem. B 2, 6474-6487
49. Polak, E. (1971) Computational methods in optimization, Academic Press, New York.
50. Ponder, J. W. and Richards, F. M. (1987) An efficient newton-like method for molecular mechanics energy minimization of large molecules J. Comput. Chem. 8, 1016-1024
51. Parr, R. and Yang, W. (1994) Density-functional theory of atoms and molecules, pp 47-86, Oxford University Press, New York.
52. Becke, A. D. (1988) Density-fnnctional exchange-energy approximation with correct asymptotic behavior Phys. Rev. A 38, 3098-3100
53. Fujii, G., Chang, J. E., Coley, T., and Steere, B. (1997) The formation of amphotericin B ion channels in lipid bilayers Biochemistry 36, 4959-4968
54. Gagos̈, M., Koper, R., and Gruszecki, W. I. (2001) Spectrophotometric analysis of organisation of dipalmitoylphosphatidylcholine bilayers containing the polyene antibiotic amphotericin B Biochim. Biophys. Acta 1511, 90-98
55. 13C CP-MAS study of the gel phases of 1,2-dipalmitoylphosphatidylcholine Biochim. Biophys. Acta 1023, 143-146
56. 31P CP-MAS NMR J. Am. Chem. Soc. 119, 6629-6637
57. Baran, M. and Mazerski, J. (2002) Molecular modelling of amphotericin B-ergosterol primary complex in water Biophys. Chem. 95, 125-133
58. Te Welscher, Y. M., ten Napel, H. H., Balagué, M. M., Souza, C. M., Riezman, H., de Kruijff, B., and Breukink, E. (2008) Natamycin blocks fungal growth by binding specifically to ergosterol without permeabilizing the membrane J. Biol. Chem. 283, 6393-6401
59. Matsumori, N., Sawada, Y., and Murata, M. (2005) Mycosamine orientation of amphotericin B controlling interaction with ergosterol: sterol-dependent activity of conformation-restricted derivatives with an amino-carbonyl bridge J. Am. Chem. Soc. 127, 10667-10675
60. Croatt, M. and Carreira, E. (2011) Probing the role of the mycosamine C2′-OH on the activity of amphotericin B Org. Lett. 13, 1390-1393
61. Silberstein, A. (1998) Conformational analysis of amphotericin B - Cholesterol channel complex J. Membr. Biol. 126, 117-126
62. Czub, J., Neumann, A., Borowski, E., and Baginski, M. (2009) Influence of a lipid bilayer on the conformational behavior of amphotericin B derivatives-A molecular dynamics study Biophys. Chem. 141, 105-116
63. Wilcock, B. C., Endo, M. M., Uno, B. E., and Burke, M. D. (2013) C2′-OH of amphotericin B plays an important role in binding the primary sterol of human cells but not yeast cells J. Am. Chem. Soc. 135, 8488-8491
64. Baginski, M., Tempczyk, A., and Browski, E. (1989) Comparative conformational analysis of cholesterol and ergosterol by molecular mechanics Eur. Biophys. J. 17, 159-166