User menu

Interaction of the macrolide antibiotic azithromycin with lipid bilayers: effect on membrane organization, fluidity, and permeability

Bibliographic reference Berquand, A. ; Fa, N. ; Dufrêne, Yves ; Mingeot-Leclercq, Marie-Paule. Interaction of the macrolide antibiotic azithromycin with lipid bilayers: effect on membrane organization, fluidity, and permeability. In: Pharmaceutical Research, Vol. 22, no. 3, p. 465-475 (2005)
Permanent URL
  1. 1. S. J. Singer and G. L. Nicolson. The fluid mosaic model of the structure of cell membranes. Science 175:720?731 (1972).
  2. 2. P. Somerharju, J. A. Virtanen, and K. H. Cheng. Lateral organisation of membrane lipids. The superlattice view. Biochim. Biophys. Acta 1440:32?48 (1999).
  3. 3. S. Pfeffer. Membrane domains in the secretory and endocytic pathways. Cell 112:507?517 (2003).
  4. 4. B. van Deurs, K. Roepstorff, A. M. Hommelgaard, and K. Sandvig. Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol. 13:92?100 (2003).
  5. 5. J. C. Holthuis, G. van Meer, and K. Huitema. Lipid microdomains, lipid translocation and the organization of intracellular membrane transport (Review). Mol. Membr. Biol. 20:231?241 (2003).
  6. 6. A. D. Dergunov, J. Taveirne, B. Vanloo, H. Caster, and M. Rosseneu. Structural organization of lipid phase and protein-lipid interface in apolipoprotein-phospholipid recombinants: influence of cholesterol. Biochim. Biophys. Acta 1346:131?146 (1997).
  7. 7. K. Jorgensen, J. H. Ipsen, O. G. Mouritsen, and M. J. Zuckermann. The effect of anaesthetics on the dynamic heterogeneity of lipid membranes. Chem. Phys. Lipids 65:205?216 (1993).
  8. 8. K. Jorgensen, J. H. Ipsen, O. G. Mouritsen, D. Bennett, and M. J. Zuckermann. The effects of density fluctuations on the partitioning of foreign molecules into lipid bilayers: application to anaesthetics and insecticides. Biochim. Biophys. Acta 1067:241?253 (1991).
  9. 9. T. Soderlund, J. Y. Lehtonen, and P. K. Kinnunen. Interactions of cyclosporin A with phospholipid membranes: effect of cholesterol. Mol. Pharmacol. 55:32?38 (1999).
  10. 10. J. J. Wenz and F. J. Barrantes. Steroid structural requirements for stabilizing or disrupting lipid domains. Biochemistry 42:14267?14276 (2003).
  11. 11. A. B. Hendrich, O. Wesolowska, and K. Michalak. Trifluoperazine induces domain formation in zwitterionic phosphatidylcholine but not in charged phosphatidylglycerol bilayers. Biochim. Biophys. Acta 1510:414?425 (2001).
  12. 12. A. Schanck, M. P. Mingeot-Leclercq, P. M. Tulkens, D. Carrier, I. C. Smith, and H. C. Jarrell. Interactions of aminoglycoside antibiotics with phospholipids. A deuterium nuclear magnetic resonance study. Chem. Phys. Lipids 62:153?163 (1992).
  13. 13. D. Tyteca, A. Schanck, Y. F. Dufrene, M. Deleu, P. J. Courtoy, P. M. Tulkens, and M. P. Mingeot-Leclercq. The macrolide antibiotic azithromycin interacts with lipids and affects membrane organization and fluidity: studies on Langmuir-Blodgett monolayers, liposomes and J774 macrophages. J. Membr. Biol. 192:203?215 (2003).
  14. 14. D. Tyteca, S. P. Van Der, M. Mettlen, F. Van Bambeke, P. M. Tulkens, M. P. Mingeot-Leclercq, and P. J. Courtoy. Azithromycin, a lysosomotropic antibiotic, has distinct effects on fluid-phase and receptor-mediated endocytosis, but does not impair phagocytosis in J774 macrophages. Exp. Cell Res. 281:86?100 (2002).
  15. 15. D. Tyteca, S. P. Van Der, F. Van Bambeke, K. Leys, P. M. Tulkens, P. J. Courtoy, and M. P. Mingeot-Leclercq. Azithromycin, a lysosomotropic antibiotic, impairs fluid-phase pinocytosis in cultured fibroblasts. Eur. J. Cell Biol. 80:466?478 (2001).
  16. 16. J. C. Hooton, C. S. German, S. Allen, M. C. Davies, C. J. Roberts, S. J. Tendler, and P. M. Williams. An atomic force microscopy study of the effect of nanoscale contact geometry and surface chemistry on the adhesion of pharmaceutical particles. Pharm. Res. 21:953?961 (2004).
  17. 17. K. Six, J. Murphy, I. Weuts, D. Q. Craig, G. Verreck, J. Peeters, M. Brewster, and M. G. Van den. Identification of phase separation in solid dispersions of itraconazole and Eudragit E100 using microthermal analysis. Pharm. Res. 20:135?138 (2003).
  18. 18. Y. F. Dufrene and G. U. Lee. Advances in the characterization of supported lipid films with the atomic force microscope. Biochim. Biophys. Acta 1509:14?41 (2000).
  19. 19. A. Engel and D. J. Muller. Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7:715?718 (2000).
  20. 20. M. P. Mingeot-Leclercq, J. Piret, R. Brasseur, and P. M. Tulkens. Effect of acidic phospholipids on the activity of lysosomal phospholipases and on their inhibition by aminoglycoside antibiotics?I. Biochemical analysis. Biochem. Pharmacol. 40:489?497 (1990).
  21. 21. R. D. Kaiser and E. London. Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth. Biochemistry 37:8180?8190 (1998).
  22. 22. B. R. Lentz. Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem. Phys. Lipids 64:99?116 (1993).
  23. 23. S. Kitagawa, M. Matsubayashi, K. Kotani, K. Usui, and F. Kametani. Asymmetry of membrane fluidity in the lipid bilayer of blood platelets: fluorescence study with diphenylhexatriene and analogs. J. Membr. Biol. 119:221?227 (1991).
  24. 24. J. N. Weinstein, S. Yoshikami, P. Henkart, R. Blumenthal, and W. A. Hagins. Liposome-cell interaction: transfer and intracellular release of a trapped fluorescent marker. Science 195:489?492 (1977).
  25. 25. F. Van Bambeke, M. P. Mingeot-Leclercq, A. Schanck, R. Brasseur, and P. M. Tulkens. Alterations in membrane permeability induced by aminoglycoside antibiotics: studies on liposomes and cultured cells. Eur. J. Pharmacol. 247:155?168 (1993).
  26. 26. G. R. Bartlett. Phosphorus assay in column chromatography. J. Biol. Chem. 234:466?468 (1959).
  27. 27. S. W. Hui, R. Viswanathan, J. A. Zasadzinski, and J. N. Israelachvili. The structure and stability of phospholipid bilayers by atomic force microscopy. Biophys. J. 68:171?178 (1995).
  28. 28. N. C. Santos, E. Ter Ovanesyan, J. A. Zasadzinski, and M. A. Castanho. Reconstitution of phospholipid bilayer by an atomic force microscope tip. Biophys. J. 75:2119?2120 (1998).
  29. 29. O. G. Mouritsen and K. Jorgensen. Dynamical order and disorder in lipid bilayers. Chem. Phys. Lipids 73:3?25 (1994).
  30. 30. M. M. Baksh, M. Jaros, and J. T. Groves. Detection of molecular interactions at membrane surfaces through colloid phase transitions. Nature 427:139?141 (2004).
  31. 31. D. A. Middleton, D. G. Reid, and A. Watts. Combined quantitative and mechanistic study of drug-membrane interactions using a novel 2H NMR approach. J. Pharm. Sci. 93:507?514 (2004).
  32. 32. C. Matos, J. L. Lima, S. Reis, A. Lopes, and M. Bastos. Interaction of antiinflammatory drugs with EPC liposomes: calorimetric study in a broad concentration range. Biophys. J. 86:946?954 (2004).
  33. 33. B. Lopez-Garcia, J. F. Marcos, C. Abad, and E. Perez-Paya. Stabilisation of mixed peptide/lipid complexes in selective antifungal hexapeptides. Biochim. Biophys. Acta 1660:131?137 (2004).
  34. 34. H. Lygre, G. Moe, and H. Holmsen. Interaction of ibuprofen with eukaryotic membrane lipids. Acta Odontol. Scand. 61:303?309 (2003).
  35. 35. P. Suomalainen, C. Johans, T. Soderlund, and P. K. Kinnunen. Surface activity profiling of drugs applied to the prediction of blood-brain barrier permeability. J. Med. Chem. 47:1783?1788 (2004).
  36. 36. A. A. Hidalgo, W. Caetano, M. Tabak, and O. N. Oliveira Jr. Interaction of two phenothiazine derivatives with phospholipid monolayers. Biophys. Chem. 109:85?104 (2004).
  37. 37. T. Harder, P. Scheiffele, P. Verkade, and K. Simons. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929?942 (1998).
  38. 38. H. W. Huang, E. M. Goldberg, and R. Zidovetzki. Ceramide induces structural defects into phosphatidylcholine bilayers and activates phospholipase A2. Biochem. Biophys. Res. Commun. 220:834?838 (1996).
  39. 39. T. Kobayashi, M. H. Beuchat, J. Chevallier, A. Makino, N. Mayran, J. M. Escola, C. Lebrand, P. Cosson, T. Kobayashi, and J. Gruenberg. Separation and characterization of late endosomal membrane domains. J. Biol. Chem. 277:32157?32164 (2002).
  40. 40. E. C. Miller and G. M. Helmkamp Jr. Exposure of phosphatidylinositol transfer proteins to sphingomyelin-cholesterol membranes suggests transient but productive interactions with raft-like, liquid-ordered domains. Biochemistry 42:13250?13259 (2003).
  41. 41. V. Schram and T. E. Thompson. Influence of the intrinsic membrane protein bacteriorhodopsin on gel-phase domain topology in two-component phase-separated bilayers. Biophys. J. 72:2217?2225 (1997).
  42. 42. K. H. Kim, T. Ahn, and C. H. Yun. Membrane properties induced by anionic phospholipids and phosphatidylethanolamine are critical for the membrane binding and catalytic activity of human cytochrome P450 3A4. Biochemistry 42:15377?15387 (2003).
  43. 43. M. L. Fanani, S. Hartel, R. G. Oliveira, and B. Maggio. Bidirectional control of sphingomyelinase activity and surface topography in lipid monolayers. Biophys. J. 83:3416?3424 (2002).
  44. 44. L. Yang and M. Glaser. Formation of membrane domains during the activation of protein kinase C. Biochemistry 35:13966?13974 (1996).
  45. 45. K. M. Maloney, M. Grandbois, C. Salesse, D. W. Grainger, and A. Reichert. Membrane microstructural templates for enzyme domain formation. J. Mol. Recognit. 9:368?374 (1996).
  46. 46. E. S. Stuart, W. C. Webley, and L. C. Norkin. Lipid rafts, caveolae, caveolin-1, and entry by Chlamydiae into host cells. Exp. Cell Res. 287:67?78 (2003).
  47. 47. W. B. Huttner and J. Zimmerberg. Implications of lipid microdomains for membrane curvature, budding and fission. Curr. Opin. Cell Biol. 13:478?484 (2001).
  48. 48. M. A. del Pozo, N. B. Alderson, W. B. Kiosses, H. H. Chiang, R. G. Anderson, and M. A. Schwartz. Integrins regulate Rac targeting by internalization of membrane domains. Science 303:839?842 (2004).
  49. 49. C. Bezombes, G. Laurent, and J. P. Jaffrezou. Implication of raft microdomains in drug induced apoptosis. Curr. Med. Chem. Anti-Canc. Agents 3:263?270 (2003).
  50. 50. G. M. Humphries and J. P. Lovejoy. Lateral phase separation of phospholipids as a basis for increased permeability of membranes towards fluorescein and other chemical species. J. Membr. Biol. 80:249?256 (1984).
  51. 51. M. A. Singer and M. K. Jain. Interaction of four local anesthetics with phospholipid bilayer membranes: permeability effects and possible mechanisms. Can. J. Biochem. 58:815?821 (1980).
  52. 52. O. G. Mouritsen and K. Jorgensen. A new look at lipid-membrane structure in relation to drug research. Pharm. Res. 15:1507?1519 (1998).
  53. 53. M. C. Giocondi, P. E. Milhiet, P. Dosset, and C. Le Grimellec. Use of cyclodextrin for AFM monitoring of model raft formation. Biophys. J. 86:861?869 (2004).
  54. 54. D. P. Siegel. Inverted micellar intermediates and the transitions between lamellar, cubic, and inverted hexagonal lipid phases. II. Implications for membrane-membrane interactions and membrane fusion. Biophys. J. 49:1171?1183 (1986).
  55. 55. M. P. Andrich and J. M. Vanderkooi. Temperature dependence of 1,6-diphenyl-1,3,5-hexatriene fluorescence in phophoslipid artificial membranes. Biochemistry 15:1257?1261 (1976).
  56. 56. B. R. Lentz, Y. Barenholz, and T. E. Thompson. Fluorescence depolarization studies of phase transitions and fluidity in phospholipid bilayers. 1. Single component phosphatidylcholine liposomes. Biochemistry 15:4521?4528 (1976).
  57. 57. B. R. Lentz, Y. Barenholz, and T. E. Thompson. Fluorescence depolarization studies of phase transitions and fluidity in phospholipid bilayers. 2 Two-component phosphatidylcholine liposomes. Biochemistry 15:4529?4537 (1976).
  58. 58. F. R. Maxfield. Plasma membrane microdomains. Curr. Opin. Cell Biol. 14:483?487 (2002).
  59. 59. C. Dietrich, L. A. Bagatolli, Z. N. Volovyk, N. L. Thompson, M. Levi, K. Jacobson, and E. Gratton. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417?1428 (2001).
  60. 60. B. J. Nichols. GM1-containing lipid rafts are depleted within clathrin-coated pits. Curr. Biol. 13:686?690 (2003).
  61. 61. P. Draber and L. Draberova. Lipid rafts in mast cell signaling. Mol. Immunol. 38:1247?1252 (2002).
  62. 62. Y. Barenholz. Cholesterol and other membrane active sterols: from membrane evolution to ?rafts?. Prog. Lipid Res. 41:1?5 (2002).
  63. 63. X. M. Li, M. M. Momsen, H. L. Brockman, and R. E. Brown. Sterol structure and sphingomyelin acyl chain length modulate lateral packing elasticity and detergent solubility in model membranes. Biophys. J. 85:3788?3801 (2003).
  64. 64. H. A. Rinia, M. M. Snel, J. P. van der Eerden, and B. de Kruijff. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501:92?96 (2001).
  65. 65. P. R. Maulik and G. G. Shipley. Interactions of N-stearoyl sphingomyelin with cholesterol and dipalmitoylphosphatidylcholine in bilayer membranes. Biophys. J. 70:2256?2265 (1996).
  66. 66. T. J. McIntosh, S. A. Simon, D. Needham, and C. H. Huang. Structure and cohesive properties of sphingomyelin/cholesterol bilayers. Biochemistry 31:2012?2020 (1992).
  67. 67. F. A. Nezil and M. Bloom. Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes. Biophys. J. 61:1176?1183 (1992).
  68. 68. D. Needham and R. S. Nunn. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:997?1009 (1990).
  69. 69. E. Evans and D. Needham. Giant vesicle bilayers composed of mixtures of lipids, cholesterol and polypeptides. Thermomechanical and (mutual) adherence properties. Faraday Discuss. Chem. Soc. 267?280 (1986).
  70. 70. J. P. Montenez, F. Van Bambeke, J. Piret, A. Schanck, R. Brasseur, P. M. Tulkens, and M. P. Mingeot-Leclercq. Interaction of the macrolide azithromycin with phospholipids. II. Biophysical and computer-aided conformational studies. Eur. J. Pharmacol. 314:215?227 (1996).
  71. 71. J. P. Montenez, F. Van Bambeke, J. Piret, R. Brasseur, P. M. Tulkens, and M. P. Mingeot-Leclercq. Interactions of macrolide antibiotics (Erythromycin A, roxithromycin, erythromycylamine [Dirithromycin], and azithromycin) with phospholipids: computer-aided conformational analysis and studies on acellular and cell culture models. Toxicol. Appl. Pharmacol. 156:129?140 (1999).
  72. 72. F. Van Bambeke, J. P. Montenez, J. Piret, P. M. Tulkens, P. J. Courtoy, and M. P. Mingeot-Leclercq. Interaction of the macrolide azithromycin with phospholipids. I. Inhibition of lysosomal phospholipase A1 activity. Eur. J. Pharmacol. 314:203?214 (1996).
  73. 73. R. Brasseur, G. Laurent, J. M. Ruysschaert, and P. Tulkens. Interactions of aminoglycoside antibiotics with negatively charged lipid layers. Biochemical and conformational studies. Biochem. Pharmacol. 33:629?637 (1984).
  74. 74. M. P. Mingeot-Leclercq, A. Schanck, M. F. Ronveaux-Dupal, M. Deleers, R. Brasseur, J. M. Ruysschaert, G. Laurent, and P. M. Tulkens. Ultrastructural, physico-chemical and conformational study of the interactions of gentamicin and bis(beta-diethylaminoethylether) hexestrol with negatively-charged phospholipid layers. Biochem. Pharmacol. 38:729?741 (1989).
  75. 75. J. L. Slater, C. H. Huang, and I. W. Levin. Interdigitated bilayer packing motifs: Raman spectroscopic studies of the eutectic phase behavior of the 1-stearoyl-2-caprylphosphatidylcholine/dimyristoyl phosphatidylcholine binary mixture. Biochim. Biophys. Acta 1106:242?250 (1992).