Self-association of amphotericin b: Spontaneous formation of molecular structures responsible for the toxic side effects of the antibiotic

Journal of Physical Chemistry B

Volumn 118, Issue 48, 2014, Pages 13821-13832

  Starzyk, Joanna ^a   Gruszecki, Marcin ^b   Tutaj, Krzysztof ^a   Luchowski, Rafal ^a   Szlazak, Radoslaw ^a   Wasko, Piotr ^a   Grudzinski, Wojciech ^a   Czub, Jacek ^c   Gruszecki, Wieslaw I ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

^b MEDICAL UNIVERSITY OF GDANSK   (Poland)

^c GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; DIMERS; ELECTROPHYSIOLOGY; MOLECULAR DYNAMICS; MOLECULAR SPECTROSCOPY; SELF ASSEMBLY;

DIMERIC STRUCTURE; ELECTRONIC ABSORPTION; MOLECULAR DYNAMIC CALCULATION; MOLECULAR ORGANIZATION; SPONTANEOUS FORMATION; STRUCTURAL DETERMINANTS; TIME-RESOLVED FLUORESCENCE; TOXIC SIDE EFFECTS;

ANTIBIOTICS;

AMPHOTERICIN B; ANTIINFECTIVE AGENT; LIPOSOME; SOLVENT;

CHEMISTRY; CIRCULAR DICHROISM; DIMERIZATION; FLUORESCENCE MICROSCOPY; HYDROGEN BOND; KINETICS; METABOLISM; MOLECULAR DYNAMICS; PH; STATIC ELECTRICITY;

AMPHOTERICIN B; ANTI-BACTERIAL AGENTS; CIRCULAR DICHROISM; DIMERIZATION; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; KINETICS; LIPOSOMES; MICROSCOPY, FLUORESCENCE; MOLECULAR DYNAMICS SIMULATION; SOLVENTS; STATIC ELECTRICITY;

EID: 84915745400     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp510245n     Document Type: Article

References (38)

1. Baginski, M.; Cybulska, B.; Gruszecki, W. I. Interaction of Macrolide Antibiotics with Lipid Membranes. In Advances in Planar Lipid Bilayers and Liposomes; Ottova-Liu, A., Ed.; Elsevier Science Publ.: Amsterdam, The Netherlands, 2006; Vol. 3, pp 269-329.
2. Mora-Duarte, J.; Betts, R.; Rotstein, C.; Colombo, A. L.; Thompson-Moya, L.; Smietana, J.; Lupinacci, R.; Sable, C.; Kartsonis, N.; Perfect, J. Comparison of Caspofungin and Amphotericin B for Invasive Candidiasis N. Engl. J. Med. 2002, 347, 2020-2029
3. Nakagawa, Y.; Umegawa, Y.; Takano, T.; Tsuchikawa, H.; Matsumori, N.; Murata, M. Effect of Sterol Side Chain on Ion Channel Formation by Amphotericin B in Lipid Bilayers Biochemistry 2014, 53, 3088-3094
4. 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. Amphotericin Forms an Extramembranous and Fungicidal Sterol Sponge Nat. Chem. Biol. 2014, 10, 400-406
5. Gray, K. C.; Palacios, D. S.; Dailey, I.; Endo, M. M.; Uno, B. E.; Wilcock, B. C.; Burke, M. D. Amphotericin Primarily Kills Yeast by Simply Binding Ergosterol Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 2234-2239
6. Gagos, M.; Arczewska, M. FTIR Spectroscopic Study of Molecular Organization of the Antibiotic Amphotericin B in Aqueous Solution and in DPPC Lipid Monolayers Containing the Sterols Cholesterol and Ergosterol Eur. Biophys J. 2012, 41, 663-673
7. De Kruijff, B.; Gerritsen, W. J.; Oerlemans, A.; Demel, R. A.; van Deenen, L. L. Polyene Antibiotic-Sterol Interactions in Membranes of Acholeplasma laidlawii Cells and Lecithin Liposomes. I. Specificity of the Membrane Permeability Changes Induced by the Polyene Antibiotics Biochim. Biophys. Acta 1974, 339, 30-43
8. Wasko, P.; Luchowski, R.; Tutaj, K.; Grudzinski, W.; Adamkiewicz, P.; Gruszecki, W. I. Toward Understanding of Toxic Side Effects of a Polyene Antibiotic Amphotericin B: Fluorescence Spectroscopy Reveals Widespread Formation of the Specific Supramolecular Structures of the Drug Mol. Pharmaceutics 2012, 9, 1511-1520
9. Gruszecki, W. I.; Gagos, M.; Herec, M.; Kernen, P. Organization of Antibiotic Amphotericin B in Model Lipid Membranes. A Mini Review Cell. Mol. Biol. Lett. 2003, 8, 161-170
10. Wojtowicz, K.; Gruszecki, W. I.; Walicka, M.; Barwicz, J. Effect of Amphotericin B on Dipalmitoylphosphatidylcholine Membranes: Calorimetry, Ultrasound Absorption and Monolayer Technique Studies Biochim. Biophys. Acta 1998, 1373, 220-226
11. Herec, M.; Dziubinska, H.; Trebacz, K.; Morzycki, J. W.; Gruszecki, W. I. An Effect of Antibiotic Amphotericin B on Ion Transport Across Model Lipid Membranes and Tonoplast Membranes Biochem. Pharmacol. 2005, 70, 668-675
12. Baginski, M.; Resat, H.; McCammon, J. A. Molecular Properties of Amphotericin B Membrane Channel: a Molecular Dynamics Simulation Mol. Pharmacol. 1997, 52, 560-570
13. Gabrielska, J.; Gagos, M.; Gubernator, J.; Gruszecki, W. I. Binding of Antibiotic Amphotericin B to Lipid membranes: a 1H NMR Study FEBS Lett. 2006, 580, 2677-2685
14. Gagos, M.; Gabrielska, J.; Dalla Serra, M.; Gruszecki, W. I. Binding of Antibiotic Amphotericin B to Lipid Membranes: Monomolecular Layer Technique and Linear Dichroism-FTIR Studies Mol. Membr. Biol. 2005, 22, 433-442
15. Toledo Grijalba, M.; Cheron, M.; Borowski, E.; Bolard, J.; Schreier, S. Modulation of Polyene Antibiotics Self-Association by Ions From the Hofmeister Series Biochim. Biophys. Acta 2006, 1760, 973-979
16. Barwicz, J.; Gruszecki, W. I.; Gruda, I. Spontaneous Organization of Amphotericin B in Aqueous Medium J. Colloid Interface Sci. 1993, 158, 71-76
17. Gagos, M.; Herec, M.; Arczewska, M.; Czernel, G.; Dalla Serra, M.; Gruszecki, W. I. Anomalously High Aggregation Level of the Polyene Antibiotic Amphotericin B in Acidic Medium: Implications for the Biological Action Biophys. Chem. 2008, 136, 44-49
18. Mazerski, J.; Bolard, J.; Borowski, E. Circular Dichroism Study of the Interaction Between Aromatic Heptaene Antibiotics and Small Unilamellar Vesicles Biochem. Biophys. Res. Commun. 1983, 116, 520-526
19. Barwicz, J.; Beauregard, M.; Tancrede, P. Circular Dichroism Study of Interactions of Fungizone or AmBisome Forms of Amphotericin B with Human Low Density Lipoproteins Biopolymers 2002, 67, 49-55
20. Gruszecki, W. I.; Gagos, M.; Herec, M. Dimers of Polyene Antibiotic Amphotericin B Detected by Means of Fluorescence Spectroscopy: Molecular Organization in Solution and in Lipid Membranes J. Photochem. Photobiol., B 2003, 69, 49-57
21. Gruszecki, W. I.; Luchowski, R.; Gagos, M.; Arczewska, M.; Sarkar, P.; Herec, M.; Mysliwa-Kurdziel, B.; Strzalka, K.; Gryczynski, I.; Gryczynski, Z. Molecular Organization of Antifungal Antibiotic Amphotericin B in Lipid Monolayers Studied by Means of Fluorescence Lifetime Imaging Microscopy Biophys Chem. 2009, 143, 95-101
22. Gagos, M.; Arczewska, M.; Gruszecki, W. I. Raman Spectroscopic Study of Aggregation Process of Antibiotic Amphotericin B Induced by H+, Na+, and K+ Ions J. Phys. Chem. B 2011, 115, 5032-5036
23. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with NAMD J. Comput. Chem. 2005, 26, 1781-1802
24. Neumann, A.; Baginski, M.; Czub, J. 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. 2010, 132, 18266-18272
25. Neumann, A.; Baginski, M.; Winczewski, S.; Czub, J. The Effect of Sterols on Amphotericin B Self-Aggregation in a Lipid Bilayer as Revealed by Free Energy Simulations Biophys. J. 2013, 104, 1485-1494
26. Neumann, A.; Czub, J.; Baginski, M. 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 2009, 113, 15875-15885
27. Feller, S. E.; Zhang, Y. H.; Pastor, R. W.; Brooks, B. R. Constant-Pressure Molecular-Dynamics Simulation-the Langevin Piston Method J. Chem. Phys. 1995, 103, 4613-4621
28. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald-an N.Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
29. Ryckaert, J. P.; Ciccotti, G.; Berendsen, H. J. C. Numerical-Integration of Cartesian Equations of Motion of a System with Constraints-Molecular-Dynamics of N-Alkanes J. Comput. Phys. 1977, 23, 327-341
30. Miyamoto, S.; Kollman, P. A. Settle-an Analytical Version of the Shake and Rattle Algorithm for Rigid Water Models J. Comput. Chem. 1992, 13, 952-962
31. Jarzembska, K. N.; Kaminski, D.; Hoser, A. A.; Malinska, M.; Senczyna, B.; Wozniak, K.; Gagos, M. Controlled Crystallization, Structure, and Molecular Properties of Iodoacetylamphotericin B Cryst. Growth Des. 2012, 12, 2336-2345
32. Gagos, M.; Gruszecki, W. I. Organization of Polyene Antibiotic Amphotericin B at the Argon-Water Interface Biophys. Chem. 2008, 137, 110-115
33. Krawczyk, S.; Jazurek, B.; Luchowski, R.; Wiacek, D. Electroabsorption Spectra of Carotenoid Isomers: Conformational Modulation of Polarizability vs. Induced Dipole Moments Chem. Phys. 2006, 326, 465-470
34. Gagos, M.; Czernel, G.; Kaminski, D. M.; Kostro, K. Spectroscopic Studies of Amphotericin B-Cu(2)+ Complexes Biometals 2011, 24, 915-922
35. Jameson, L. P.; Dzyuba, S. V. Circular Dichroism Studies on Intermolecular Interactions of Amphotericin B in Ionic Liquid-Rich Environments Chirality 2013, 25, 427-432
36. Cantor, C. R.; Schimmel, P. R. Biophysical Chemistry. Part II Techniques for the Study of Biological Structure and Function; W.H. Freeman and Company: New York, 1998.
37. Mazerski, J.; Borowski, E. Molecular Dynamics of Amphotericin B. II. Dimer in Water Biophys Chem. 1996, 57, 205-217
38. Man, D.; Olchawa, R. Two-step Impact of Amphotericin B (AmB) on Lipid Membranes: ESR Experiment and Computer Simulations J. Liposome Res. 2013, 23, 327-335