Comparative study of the AT1 receptor prodrug antagonist candesartan cilexetil with other sartans on the interactions with membrane bilayers

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 12, 2012, Pages 3107-3120

  Fotakis, Charalambos ^a,b   Megariotis, Grigorios ^b   Christodouleas, Dionysios ^a   Kritsi, Eftichia ^a,b   Zoumpoulakis, Panagiotis ^b   Ntountaniotis, Dimitrios ^a,b   Zervou, Maria ^b   Potamitis, Constantinos ^b   Hodzic, Aden ^c,d   Pabst, Georg ^c   Rappolt, Michael ^c   Mali, Gregor ^e,f   Baldus, Johanna ^g   Glaubitz, Clemens ^g   Papadopoulos, Manthos G ^b   Afantitis, Antreas ^h   Melagraki, Georgia ^h   Mavromoustakos, Thomas ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b INSTITUTE OF BIOLOGY   (Greece)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d RESEARCH CENTER PHARMACEUTICAL ENGINEERING GMBH   (Austria)

^e NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^f EN FIST CENTRE OF EXCELLENCE   (Slovenia)

^g GOETHE UNIVERSITY   (Germany)

^h NOVAMECHANICS LTD   (Cyprus)

Author keywords

Candesartan cilexetil; Differential scanning calorimetry; Molecular dynamics; Raman spectroscopy; Small angle X ray scattering; Solid state NMR

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; CANDESARTAN; CANDESARTAN HEXETIL; OLMESARTAN; SARTAN DERIVATIVE; VALSARTAN;

AB INITIO CALCULATION; ARTICLE; BILAYER MEMBRANE; CARBON NUCLEAR MAGNETIC RESONANCE; CHEMICAL INTERACTION; COMPUTER MODEL; CONFORMATION; DIFFERENTIAL SCANNING CALORIMETRY; DRUG STRUCTURE; HYDROPHOBICITY; LIPID BILAYER; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAMAN SPECTROMETRY; X RAY CRYSTALLOGRAPHY;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; BENZIMIDAZOLES; BIPHENYL COMPOUNDS; CELL MEMBRANE; IMIDAZOLES; LIPID BILAYERS; MOLECULAR CONFORMATION; RECEPTOR, ANGIOTENSIN, TYPE 1; TETRAZOLES; THERMODYNAMICS; VALINE;

EID: 84865589426     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.08.009     Document Type: Article

References (90)

1. T. Mavromoustakos, A. Kolocouris, M. Zervou, P. Roumelioti, J.M. Matsoukas, and R. Weisemann An effort to understand the molecular basis of hypertension through the study of conformational analysis of losartan and sarmesin using a combination of Nuclear Magnetic Resonance spectroscopy and theoretical calculations J. Med. Chem. 42 1999 1714 1722
2. M. De Gasparo, K.J. Catt, T. Inagami, J.W. Wright, and Th. Unger International Union of Pharmacology. XXIII. The angiotensin II receptors Pharmacol. Rev. 52 2000 415 472
3. P. Zoumpoulakis, I. Daliani, M. Zervou, I. Kyrikou, E. Siapi, G. Lamprinidis, E. Mikros, and T. Mavromoustakos Losartan's molecular basis of interaction with membranes and AT1 receptor Chem. Phys. Lipids 125 2003 13 25
4. M. Lucio, J.L.F.C. Lima, and S. Reis Drug-membrane interactions: significance for medicinal chemistry Curr. Med. Chem. 17 2010 1795 1809
5. A.M. Seddon, D. Casey, R.V. Law, A. Gee, R.H. Templer, and O. Ces Drug interactions with lipid membranes Chem. Soc. Rev. 38 2009 2509 2519
6. L.J. Wagenaar, A.A. Voors, H. Buikema, A. Van Buiten, R.H. Lübeck, P.W. Boonstra, D.J. Van Veldhuisen, and W.H. Van Gilst Functional antagonism of different angiotensin II type I receptor blockers in human arteries Cardiovasc. Drugs Ther. 16 2002 311 316
7. C. Fotakis, D. Christodouleas, P. Zoumpoulakis, E. Kritsi, N.P. Benetis, T. Mavromoustakos, H. Reis, A. Gili, M.G. Papadopoulos, and M. Zervou Comparative biophysical studies of sartan class drug molecules losartan and candesartan (CV-11974) with membrane bilayers J. Phys. Chem. B 115 2011 6180 6192
8. T.R. Oliveira, M.T. Lamy, U.M. De Paula, L.L. Guimarães, M.S. Toledo, H.K. Takahashi, A.H. Straus, C.J. Lindsey, and T.B. Paiva Structural properties of lipid reconstructs and lipid composition of normotensive and hypertensive rat vascular smooth muscle cell membranes Braz. J. Med. Biol. Res. 42 2009 844 853
9. T.J. Netticadan, T.F. Ashavaid, and K.G. Nair Characterisation of the canine cardiac sarcolemma in experimental myocardial ischemia Indian J. Clin. Biochem. 12 1997 49 54
10. R. Koynova, and M. Caffrey Phases and phase transitions of the phosphatidylcholines Biochim. Biophys. Acta 1376 1998 91 145
11. S. Tristram-Nagle, M.C. Wiener, C.P. Yang, and J.F. Nagle Kinetics of the subtransition in dipalmitoylphosphatidylcholine Biochemistry 26 1987 4288 4294
12. M.D. Housley, and K.K. Stanley Dynamics of Biological Membranes 1982 John Wiley and Sons New York
13. R.P. Rand, D. Chapman, and K. Larsson Tilted hydrocarbon chains of dipalmitoyl lecithin become perpendicular to the bilayer before melting Biophys. J. 15 1975 1117 1124
14. J. Stamatoff, B. Feuer, H.J. Guggenheim, G. Tellez, and T. Yamane Amplitude of rippling in the P beta phase of dipalmitoylphosphatidylcholine bilayers Biophys. J. 38 1982 217 226
15. T.J. McIntosh Differences in hydrocarbon chain tilt between hydrated phosphatidylethanolamine and phosphatidylcholine bilayer. A molecular packing model Biophys. J. 29 1980 237 245
16. N.B. Colthulp, L.H. Daly, and S.E. Wiberley Introduction to Infrared and Raman Spectroscopy 1990 Academic Press
17. C.H. Huang, J.R. Lapides, and I.W. Levin Phase-transition behaviour of saturated, symmetric chain phospholipid bilayers dispersions determined by Raman spectroscopy: correlation between spectral and thermodynamic parameters J. Am. Chem. Soc. 104 1982 5926 5930
18. I.W. Levin, and R.N. Lewis Fourier transform Raman spectroscopy of biological materials Anal. Chem. 62 1990 1101A 1111A
19. G. Pabst, M. Rappolt, H. Amenitsch, and P. Laggner Structural information from multilamellar liposomes at full hydration: full q-range fitting with high quality X-ray data Phys. Rev. E 62 2000 4000 4009
20. P. Tosco, B. Rolando, R. Fruttero, Y. Henchoz, S. Martel, P.A. Carrupt, and A. Gasco Physicochemical profiling of sartans: a detailed study of ionization constants and distribution coefficients Helv. Chim. Acta 91 2008 468 482
21. A. Ramamoorthy Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights Solid State Nucl. Magn. Reson. 35 2009 201 207
22. H. Jerebek, G. Pabst, M. Rappolt, and T. Stockner Membrane-mediated effect on ion channels induced by the anesthetic drug ketamine J. Am. Chem. Soc. 132 2010 7990 7997
23. R.S. Cantor Lipid composition and the lateral pressure profile in bilayers Biophys. J. 76 1999 2625 2639
24. C. Xing, O.H.S. Ollila, I. Vattulainen, and R. Faller Asymmetric nature of lateral pressure profiles in supported lipid membranes and its implications for membrane protein functions Soft Matter 5 2009 3258 3261
25. C. Potamitis, P. Chatzigeorgiou, E. Siapi, K. Viras, T. Mavromoustakos, A. Hodzic, G. Pabst, F. Cacho-Nerin, P. Laggner, and M. Rappolt Interactions of the AT1 antagonist valsartan with dipalmitoyl-phosphatidylcholine bilayers Biochim. Biophys. Acta 1808 2011 1753 1763
26. C. Fotakis, D. Christodouleas, P. Chatzigeorgiou, M. Zervou, N.-P. Benetis, K. Viras, and T. Mavromoustakos Development of a CP 31P NMR broadline simulation methodology for studying the interactions of antihypertensive AT1 antagonist losartan with phospholipid bilayers Biophys. J. 96 2009 2227 2236
27. D. Ntountaniotis, G. Mali, S.G. Grdadolnik, M. Halabalaki, A.-L. Skaltsounis, C. Potamitis, E. Siapi, P. Chatzigeorgiou, M. Rappolt, and T. Mavromoustakos Thermal, dynamic and structural properties of drug AT1 antagonist olmesartan in lipid bilayers Biochim. Biophys. Acta 1808 2011 2995 3006
28. I. Kyrikou, N.P. Benetis, P. Chatzigeorgiou, M. Zervou, K. Viras, C. Poulos, and T. Mavromoustakos Interactions of the dipeptide paralysin β-Ala-Tyr and the aminoacid Glu with phospholipid bilayers Biochim. Biophys. Acta 1778 2008 113 124
29. T.M. Mavromoustakos The use of differential scanning calorimetry to study drug-membrane interactions Meth. Mol. Biol. 400 2007 587 600
30. A. Hodzic, M. Rappolt, H. Amenitsch, and G. Pabst Differential modulation of membrane structure and fluctuations by plant sterols and cholesterol Biophys. J. 94 2008 3935 3944
31. T. Mavromoustakos, P. Chatzigeorgiou, C. Koukoulitsa, and S. Durdagi Partial interdigitation of lipid bilayers Int. J. Quantum Chem. 111 2011 1172 1183
32. U. Holzgrabe, I. Wawer, and B. Diehl NMR Spectroscopy in Pharmaceutical Analysis 2008 Elsevier Amsterdam
33. C. Song, H. Holmsen, and W. Nerdal Existence of lipid microdomains in bilayer of dipalmitoyl phosphatidylcholine (DPPC) and 1-stearoyl-2- docosahexenoyl phosphatidylserine (SDPS) and their perturbation by chlorpromazine: a 13C and 31P solid-state NMR study Biophys. Chem. 120 2006 178 187
34. T. Mavromoustakos, and I. Daliani Effects of cannabinoids in membrane bilayers containing cholesterol Biochim. Biophys. Acta 1420 1999 252 265
35. T. Mavromoustakos, and E. Theodoropoulou A combined use of 13C-cross polarization/magic angle spinning, 13C-magic angle spinning and 31P-nuclear magnetic resonance spectroscopy with differential scanning calorimetry to study cannabinoid-membrane interactions Chem. Phys. Lipids 92 1998 37 52
36. C. Fotakis, S. Gega, E. Siapi, C. Potamitis, K. Viras, P. Moutevelis-Minakakis, C.G. Kokotos, S. Durdagi, S. Golic Grdadolnik, B. Sartori, M. Rappolt, and T. Mavromoustakos Interactions at the bilayer interface and receptor site induced by the novel synthetic pyrrolidinone analog MMK3 Biochim. Biophys. Acta 1768 2010 422 432
37. H. Amenitsch, M. Rappolt, M. Kriechbaum, H. Mio, P. Laggner, and S. Bernstorff First performance assessment of the small-angle X-ray scattering beamline at ELETTRA J. Synchrotron Radiat. 5 1998 506 508
38. A. Caillé Remarques sur la diffusion des rayons X dans les smectiques A C. R. Acad. Sci. Paris B 274 1972 891 893
39. R. Zhang, S. Tristram-Nagle, W. Sun, R.L. Headrick, T.C. Irving, R.M. Suter, and J.F. Nagle Small-angle X-ray scattering from lipid bilayers is well described by modified Caillé theory but not by paracrystalline theory Biophys. J. 70 1996 349 357
40. M. Rappolt Bilayer thickness estimations with poor diffraction data J. Appl. Phys. 107 2010 084701-1 084701-7
41. J.F. Nagle, and S. Tristram-Nagle Structure and interactions of lipid bilayer: role of fluctuations J. Katsaras, T. Gutberlet, Lipid Bilayers. Structure and Interactions 2000 Springer Berlin 1 23
42. J.F. Nagle, and S. Tristram-Nagle Structure of lipid bilayers Biochim. Biophys. Acta 1469 2000 159 195
43. S.W. Chiu, E. Jakobsson, R.J. Mashl, and H.L. Scott Cholesterol-induced modifications in lipid bilayers: a simulation study Biophys. J. 83 2002 1842 1853
44. J.J.P. Stewart Application of the PM6 method to modeling the solid state J. Mol. Model. 14 2008 499 535
45. J.J.P. Stewart Optimization of parameters for semiempirical methods V: modification of NDDO approximations and application to 70 elements J. Mol. Model. 13 2007 1173 1213
46. G. Melagraki, A. Afantitis, H. Sarimveis, P.A. Koutentis, G. Kollias, and O. Igglessi-Markopoulou Predictive QSAR workflow for the in silico identification and screening of novel HDAC inhibitors Mol. Divers. 13 2009 301 311
47. T. Puzyn, N. Suzuki, M. Haranczyk, and J. Rak Calculation of quantum-mechanical descriptors for QSPR at the DFT level: is it necessary? J. Chem. Inf. Model. 48 2008 1174 1180
48. A. Klamt, and G. Schüürmann COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient J. Chem. Soc., Perkin Trans. 2 1993 799 805
49. J.S. Puranen, M.J. Vainio, and M.S. Johnson Accurate conformation- dependent molecular electrostatic potentials for high-throughput in silico drug discovery J. Comput. Chem. 31 2010 1722 1732
50. J.B. Klauda, R.M. Venable, J.A. Freites, J.W. O'Connor, D.J. Tobias, C. Mondragon-Ramirez, I. Vorobyov, J. MacKerell, and R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
51. R.W. Pastor, and A.D. MacKerell Development of the CHARMM force field for lipids J. Phys. Chem. Lett. 2 2011 1526 1532
52. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
53. V. Zoete, M.A. Cuendet, A. Grosdidier, and O. Michielin SwissParam: a fast force field generation tool for small organic molecules J. Comput. Chem. 32 2011 2359 2368
54. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
55. T.A. Halgren Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94 J. Comput. Chem. 17 1996 490 519
56. H.J.C. Berendsen, J.P.M. Postma, W.F. Van Gunsteren, A. Dinola, and J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
57. U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
58. S. Kumar, J.M. Rosenberg, D. Bouzida, R.H. Swendsen, and P.A. Kollman The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13 1992 1011 1021
59. J.S. Hub, B.L. De Groot, and D. van der Spoel G-whams - a free Weighted Histogram Analysis implementation including robust error and autocorrelation estimates J. Chem. Theory Comput. 6 2010 3713 3720
60. E.B. Kim, N. Lockwood, M. Chopra, O. Guzmán, N.L. Abbott, and J.J. De Pablo Interactions of liquid crystal-forming molecules with phospholipid bilayers studied by molecular dynamics simulations Biophys. J. 89 2005 3141 3158
61. J.A. Lemkul, and D.R. Bevan Assessing the stability of Alzheimer's amyloid protofibrils using molecular dynamics J. Phys. Chem. B 114 2010 1652 1660
62. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
63. R.K. Bista, R.F. Bruch, and A.M. Covington Variable-temperature Raman spectro-microscopy for a comprehensive analysis of the conformational order in PEGylated lipids J. Raman Spectrosc. 40 2008 463 471
64. J.R. Silvius, M. Lyons, P.L. Yeagle, and T.J. O'Leary Thermotropic properties of bilayers containing blanched-chain phospholipids, calorimetric, Raman and 31P NMR studies Biochemistry 24 1985 5388 5395
65. T.J. O'Leary, P.D. Ross, and I.W. Levin Effects of anesthetic and nonanesthetic steroids on dipalmitoylphosphatidylcholine liposomes: a calorimetric and Raman spectroscopic investigation Biochemistry 23 1984 4636 4641
66. T.J. O'Leary, and I.W. Levin Raman spectroscopic study of an interdigitated lipid bilayer dipalmitoylphosphatidylcholine dispersed in glycerol Biochim. Biophys. Acta 776 1984 185 189
67. R. Hosemann, and S.N. Bagchi Direct Analysis of Diffraction by Matter 1962 North-Holland Publ. Co. Amsterdam
68. H.I. Petrache, N. Gouliaev, S. Tristram-Nagle, R.T. Zhang, R.M. Suter, and J.F. Nagle Interbilayer interactions from high-resolution X-ray scattering Phys. Rev. E 57 1998 7014 7024
69. W.J. Sun, R.M. Suter, M.A. Knewtson, C.R. Worthington, S. Tristram-Nagle, R. Zhang, and J.F. Nagle Order and disorder in fully hydrated unoriented bilayers of gel phase dipalmitoylphosphatidylcholine Phys. Rev. E 49 1994 4665 4676
70. K.P. Soteriadou, A.K. Tzinia, E. Panou-Pamonis, V. Tsikaris, M. Sakarellos-Daitsiotis, C. Sakarellos, Y. Papapoulou, and R. Matsas Antigenicity and conformational analysis of the Zn2+-binding sites of two Zn2+-metalloproteases: Leishmania gp63 and mammalian endopeptidase-24.11 Biochem. J. 313 1996 455 466
71. P. Zoumpoulakis, S.G. Grdadolnik, J.M. Matsoukas, and T. Mavromoustakos Structure elucidation and conformational properties of eprosartan a non peptide Angiotensin II AT1 antagonist J. Pharm. Biomed. Anal. 28 2002 125 135
72. P. Zoumpoulakis, A. Zoga, P. Roumelioti, N. Giatas, S.G. Grdadolnik, E. Iliodromitis, D. Vlahakos, D. Kremastinos, J.M. Matsoukas, and T. Mavromoustakos Conformational and biological studies for a pair of novel synthetic AT1 antagonists. Stereoelectronic requirements for antihypertensive efficacy J. Pharm. Biomed. Anal. 31 2003 833 844
73. P. Zoumpoulakis, A. Politi, S.G. Grdadolnik, J.M. Matsoukas, and T. Mavromoustakos Structure elucidation and conformational study of V8. A novel synthetic non peptide AT1 antagonist J. Pharm. Biomed. Anal. 40 2006 1097 1104
74. C. Neale, W.F.D. Bennett, D.P. Tieleman, and R. Pomes Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers J. Chem. Theory Comput. 7 2011 4175 4188
75. G. Pabst, H. Amenitsch, D.P. Kharakoz, P. Laggner, and M. Rappolt Structure and fluctuations of phosphatidylcholines in the vicinity of the main phase transition Phys. Rev. E 70 2004 021908-1 021908-9
76. J.F. Nagle, and D.A. Wilkinson Lecithin bilayers. Density measurements and molecular interactions Biophys. J. 23 1978 159 175
77. T. Heimburg A model for the lipid pretransition: coupling of ripple formation with the chain-melting transition Biophys. J. 78 2000 1154 1165
78. M. Rappolt, G. Pabst, G. Rapp, M. Kriechbaum, H. Amenitsch, C. Krenn, S. Bernstorff, and P. Laggner New evidence for gel-liquid crystalline phase coexistence in the ripple phase of phosphatidylcholines Eur. Biophys. J. 29 2000 125 133
79. K. Sengupta, V.A. Raghunathan, and J. Katsaras Novel structural features of the ripple phase of phospholipids Europhys. Lett. 49 2000 722 728
80. E. Theodoropoulou, and D. Marsh Interactions of angiotensin II non-peptide AT1 antagonist losartan with phospholipid membranes studied by combined use of differential scanning calorimetry and electron spin resonance spectroscopy Biochim. Biophys. Acta 1461 1999 135 146
81. T. Mavromoustakos, P. Zoumpoulakis, I. Kyrikou, A. Zoga, E. Siapi, M. Zervou, I. Daliani, D. Dimitriou, A. Pitsasa, C. Kamoutsis, and P. Laggner Efforts to understand the molecular basis of hypertension through drug:membrane interactions Curr. Top. Med. Chem. 4 2004 445 459
82. M.J. Ruocco, and G.G. Shipley Characterization of the sub-transition of hydrated dipalmitoylphosphatidylcholine bilayers. Kinetic, hydration and structural study Biochim. Biophys. Acta 691 1982 309 320
83. E.S. Rowe, and T.A. Cutrera Differential scanning calorimetric studies of ethanol interactions with distearoylphosphatidylcholine: transition to the interdigitated phase Biochemistry 29 1990 10398 10404
84. E. Cagigal, L. Gonzalez, R.M. Alonso, and R.M. Jimenez pKa determination of angiotensin II receptor antagonists (ARA II) by spectrofluorimetry J. Pharm. Biomed. Anal. 26 2001 477 486
85. A. Hodzic, P. Zoumpoulakis, G. Pabst, T. Mavromoustakos, and M. Rappolt Losartan's affinity to fluid bilayers modulates lipid-cholesterol interactions Phys. Chem. Chem. Phys. 14 2012 4780 4788
86. A. Siarheyeva, J.J. Lopez, and C. Glaubitz Localization of multidrug transporter substrates within model membranes Biochemistry 45 2006 6203 6211
87. X. Tian, S. Pavlopoulos, D.P. Yang, and A. Makriyannis The interaction of cannabinoid receptor agonists, CP55940 and WIN55212-2 with membranes using solid state 2H NMR Biochim. Biophys. Acta Biomembr. 1808 2011 2095 2101
88. D.G. Rhodes, J.G. Sarmiento, and L.G. Herbette The membrane bilayer pathway Mol. Pharmacol. 27 1985 612 623
89. D.P. Hurst, A. Grossfield, D.L. Lynch, S. Feller, T.D. Romo, K. Gawrisch, M.C. Pitman, and P.H. Reggio A lipid pathway for ligand binding is necessary for a cannabinoid G protein-coupled receptor J. Biol. Chem. 285 2010 17954 17964
90. R.O. Dror, A.C. Pan, D.H. Arlow, D.W. Borhani, P. Maragakis, Y. Shan, H. Xu, and D.E. Shaw Pathway and mechanism of drug binding to G-protein-coupled receptors Proc. Natl. Acad. Sci. U. S. A. 108 2011 13118 13123