Effects of the antimalarial drug primaquine on the dynamic structure of lipid model membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 1, 2011, Pages 55-64

  Basso, Luis G M ^a   Rodrigues, Renata Z ^a   Naal, Rose M Z G ^a,b   Costa Filho, Antonio J ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Instituto Nacional de Ciencia e Tecnologia de Bioanalitica   (Brazil)

Author keywords

Calorimetry; Electron spin resonance; Model membrane; Primaquine

Indexed keywords

AMPHOLYTE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; LIPOSOME; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PRIMAQUINE;

ARTICLE; ARTIFICIAL MEMBRANE; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DRUG MECHANISM; ELECTRON SPIN RESONANCE; ENTHALPY; HUMAN; HYDROPHOBICITY; LIPID BILAYER; LIPID MEMBRANE; MALARIA; MEMBRANE FLUIDITY; PH; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; THERMOGRAPHY;

ANTIMALARIALS; CALORIMETRY; CALORIMETRY, DIFFERENTIAL SCANNING; CATIONS; DIMYRISTOYLPHOSPHATIDYLCHOLINE; ELECTRON SPIN RESONANCE SPECTROSCOPY; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; LIPIDS; MEMBRANES, ARTIFICIAL; PHOSPHOLIPIDS; PRIMAQUINE; TEMPERATURE;

EID: 78649776872     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.08.009     Document Type: Article

References (87)

1. WHO World Malaria Report 2008 World Health Organization Geneva
2. L. Povinelli, B.C. Fox, M.E. Parise, T.A. Monson, J.M. Morrisey, and A.B. Vaidya Plasmodium vivax malaria in spite of atovaquone/proguanil (Malarone) prophylaxis J. Travel Med. 10 2003 353 355
3. D.F. Clyde Clinical problems associated with the use of primaquine as a tissue schizontocidal and gametocytocidal drug Bull. World Health Organ. 59 1981 391 395
4. R.E. Coleman, A.M. Clavin, and W.K. Milhous Gametocytocidal and sporontocidal activity of antimalarials against Plasmodium berghei ANKA in ICR mice and Anopheles stephensi mosquitoes Am. J. Trop. Med. Hyg. 46 1992 169 182
5. E. Beutler The genetics of glucose-6-phosphate dehydrogenase deficiency Semin. Hematol. 27 1990 137 164
6. J.K. Baird, and K.H. Rieckmann Can primaquine therapy for vivax malaria be improved? Trends Parasitol. 19 2003 115 120
7. G. Cohen, and P. Hochstein Generation of hydrogen peroxide in erythrocytes by hemolytic agents Biochemistry 3 1964 895 900
8. Z.S. Bowman, J.D. Morrow, D.J. Jollow, and D.C. McMillan Primaquine-induced hemolytic anemia: role of membrane lipid peroxidation and cytoskeletal protein alterations in the hemotoxicity of 5-hydroxyprimaquine J. Pharmacol. Exp. Ther. 314 2005 838 845
9. L.J.C. Bolchoz, A.K. Gelasco, D.J. Jollow, and D.C. McMillan Primaquine-induced hemolytic anemia: formation of free radicals in rat erythrocytes exposed to 6-methoxy-8-hydroxylaminoquinoline J. Pharmacol. Exp. Ther. 303 2002 1121 1129
10. J. Vásquez-Vivar, and O. Augusto Hydroxylated metabolites of the antimalarial drug primaquine. Oxidation and redox cycling J. Biol. Chem. 267 1992 6848 6854
11. M. Luxnat, and H.J. Galla Partition of chlorpromazine into lipid bilayer membranes: the effect of membrane structure and composition Biochim. Biophys. Acta 856 1986 274 282
12. 2+)-ATPase Biochim. Biophys. Acta 732 1983 428 440
13. K. Nicolay, and B. Dekruijff Effects of adriamycin on respiratory chain activities in mitochondria from rat liver, rat heart and bovine heart. Evidence for a preferential inhibition of complex III and IV Biochim. Biophys. Acta 892 1987 320 330
14. R. Kumar, O. Holian, B. Cook, and P. Roshani Inhibition of rat brain protein kinase C by lipid soluble psychotropics Neurochem. Res. 22 1997 1 10
15. R. Krivanek, L. Okoro, and R. Winter Effect of cholesterol and ergosterol on the compressibility and volume fluctuations of phospholipid-sterol bilayers in the critical point region: a molecular acoustic and calorimetric study Biophys. J. 94 2008 3538 3548
16. L.Y. Lim, and M.L. Go The antimalarial agent halofantrine perturbs phosphatidylcholine and phosphatidylethanolamine bilayers: a differential scanning calorimetric study Chem. Pharm. Bull. 47 1999 732 737
17. S.G. Couto, M.C. Nonato, and A.J. Costa-Filho Defects in vesicle core induced by Escherichia coli dihydroorotate dehydrogenase Biophys. J. 94 2008 1746 1753
18. Y.K. Shin, C. Levinthal, F. Levinthal, and W.L. Hubbel Colicin E1 binding to membranes: time-resolved studies of spin-labeled mutants Science 259 1993 960 963
19. P.P. Borbat, A.J. Costa-Filho, K.A. Earle, J.K. Moscicki, and J.H. Freed Electron spin resonance in studies of membranes and proteins Science 291 2001 266 269
20. H. Heerklotz, and J. Seelig Application of pressure perturbation calorimetry to lipid bilayers Biophys. J. 82 2002 1445 1452
21. J.H. Freed Theory of slow tumbling ESR spectra for nitroxides 1976 Academic Press New York
22. D.J. Schneider, and J.H. Freed Calculating slow motional magnetic resonance spectra: a user's guide 1989 Plenum Publishing New York
23. D.E. Budil, S. Lee, S. Saxena, and J.H. Freed Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm J. Magn. Reson. A 120 1996 155 189
24. A. Ferrarini, P.L. Nordio, G.J. Moro, R.H. Crepeau, and J.H. Freed A theoretical model of phospholipid dynamics in membranes J. Chem. Phys. 91 1989 5707 5721
25. A.P.S. Citadini, A.P.A. Pinto, A.P.U. Araujo, O.R. Nascimento, and A.J. Costa-Filho EPR studies of chlorocatechol 1, 2-dioxygenase: Evidences of iron reduction during catalysis and of the binding of amphipatic molecules Biophys. J. 88 2005 3502 3508
26. L. Kar, E. Neyigner, and J.H. Freed Electron spin resonance and electron-spin-echo study of oriented multilayers of L-α- dipalmitoylphosphatidylcholine water systems Biophys. J. 48 1985 569 595
27. E. Meirovitch, A. Nayeem, and J.H. Freed Analysis of protein-lipid interactions based on model simulations of electron spin resonance spectra J. Phys. Chem. 88 1984 3454 3465
28. K.A. Earle, J.K. Moscicki, M.T. Ge, D.E. Budil, and J.H. Freed 250-GHz electron spin resonance studies of polarity gradients along the aliphatic chains in phospholipid membranes Biophys. J. 66 1994 1213 1221
29. D. Marsh, CRC Press, Boca Raton, Handbook of Lipid Bilayers, 1990.
30. D. Marsh, A. Watts, and P.F. Knowles Cooperativity of the phase transition in single- and multibilayer lipid vesicles Biochim. Biophys. Acta 465 1977 500 514
31. M.I. Kanehisa, and T.Y. Tsong Cluster model of lipid phase transitions with application to passive permeation of molecules and structure relaxations in lipid bilayers J. Am. Chem. Soc. 100 1978 424 432
32. T.Y. Tsong, M. Greenberg, and M.I. Kanehisa Anesthetic action on membrane lipids Biochemistry 16 1977 3115 3121
33. S.M. Gruner Stability of lyotropic phases with curved interfaces J. Phys. Chem. 93 1989 7562 7570
34. R.M. Epand, and R. Bottega Modulation of the phase transition behavior of phosphatidylethanolamine by cholesterol and oxysterols Biochemistry 26 1987 1820 1825
35. 2H-nuclear magnetic resonance Biophys. J. 56 1989 1037 1041
36. 2H NMR experiments Eur. Biophys. J. 36 2007 919 931
37. R.M. Epand, and D.S. Lester The role of membrane biophysical properties in the regulation of protein kinase C activity Trends Pharmacol. Sci. 11 1990 317 320
38. P. Hildebrandt, T. Heimburg, and D. Marsh Quantitative conformational analysis of cytochrome C bound to phospholipid vesicles studied by resonance Raman spectroscopy Eur. Biophys. J. 18 1990 193 201
39. M.J. Janiak, D.M. Small, and G.G. Shipley Nature of the thermal pretransition of synthetic phospholipids: dimyristolyl- and dipalmitoyllecithin Biochemistry 15 1976 4575 4580
40. B.D. Ladbrooke, and D. Chapman Thermal analysis of lipids, proteins and biological membranes. A review and summary of some recent studies Chem. Phys. Lipids 3 1969 304 356
41. G. Cevc Polymorphism of the bilayer membranes in the ordered phase and the molecular origin of the lipid pretransition and rippled lamellae Biochim. Biophys. Acta 1062 1991 59 69
42. J.M. Carlson, and J.P. Sethna Theory of the ripple phase in hydrated phospholipid bilayers Phys. Rev. A 36 1987 3359 3374
43. K. Gardikis, S. Hatziantoniou, K. Viras, M. Wagner, and C. Demetzos A DSC and Raman spectroscopy study on the effect of PAMAM dendrimer on DPPC model lipid membranes Int. J. Pharm. 318 2006 118 123
44. E.J. Prenner, R.N.A.H. Lewis, L.H. Kondejewski, R.S. Hodges, and R.N. McElhaney Differential scanning calorimetric study of the effect of the antimicrobial peptide gramicidin S on the thermotropic phase behavior of phosphatidylcholine, phosphatidylethanolamine and phosphatidylglycerol lipid bilayer membranes Biochim. Biophys. Acta Biomembr. 1417 1999 211 223
45. L. Okoro, and R. Winter Pressure perturbation calorimetric studies on phospholipid-sterol mixtures Z. Naturforsch. B 63b 2008 769 778
46. C. Bernsdorff, and R. Winter Differential properties of the sterols cholesterol, ergosterol, β-sitosterol, trans-7-dehydrocholesterol, stigmasterol and lanosterol on DPPC bilayer order J. Phys. Chem. B 107 2003 10658 10664
47. D.P. Siegel, and R.M. Epand Effect of influenza hemagglutinin fusion peptide on lamellar/inverted phase transitions in dipalmitoleoylphosphatidylethanolamine: implications for membrane fusion mechanisms Biochim. Biophys. Acta Biomembr. 1468 2000 87 98
48. W.R. Perkins, R.B. Dause, R.A. Parente, S.R. Minchey, K.C. Neuman, S.M. Gruner, T.F. Taraschi, and A.S. Janoff Role of lipid polymorphism in pulmonary surfactant Science 273 1996 330 332
49. B. deKruijff Biomembranes - lipids beyond the bilayer Nature 386 1997 129 130
50. S.M. Gruner Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids Proc. Natl. Acad. Sci. U.S.A. 82 1985 3665 3669
51. J.R. Giorgione, R. Kraayenhof, and R.M. Epand Interfacial membrane properties modulate protein kinase C activation: role of the position of acyl chain unsaturation Biochemistry 37 1998 10956 10960
52. S.M.A. Davies, R.M. Epand, R. Kraayenhof, and R.B. Cornell Regulation of CTP: phosphocholine cytidylyltransferase activity by the physical properties of lipid membranes: an important role for stored curvature strain energy Biochemistry 40 2001 10522 10531
53. K.J. Hallock, D.K. Lee, and A. Ramamoorthy MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain Biophys. J. 84 2003 3052 3060
54. J. Barry, M. Fritz, J.R. Brender, P.E.S. Smith, D.K. Lee, and A. Ramamoorthy Determining the effects of lipophilic drugs on membrane structure by solid-state NMR spectroscopy: the case of the antioxidant curcumin J. Am. Chem. Soc. 131 2009 4490 4498
55. A.G. Lee Lipid phase transitions and phase diagrams II. Mixtures involving lipids Biochim. Biophys. Acta 472 1977 285 344
56. O.G. Mouritsen, and M. Bloom Mattress model of lipid-protein interactions in membranes Biophys. J. 46 1984 141 153
57. K. Sengupta, V.A. Raghunathan, and J. Katsaras Structure of the ripple phase of phospholipid multibilayers Phys. Rev. E 68 2003 1 12
58. β′ in hydrated phosphatidylcholine multimembranes Phys. Rev. Lett. 66 1991 903 906
59. A.H. deVries, S. Yefimov, A.E. Mark, and S.J. Marrink Molecular structure of the lecithin ripple phase Proc. Natl. Acad. Sci. U.S.A. 102 2005 5392 5396
60. D. Marsh Molecular motion in phospholipid bilayers in the gel phase: Long axis rotation Biochemistry 19 1980 1632 1637
61. R.J. Wittebort, A. Blume, T.H. Huang, S.K. DasGupta, and R.G. Griffin Carbon-13 nuclear magnetic resonance investigations of phase transitions and phase equilibria in pure and mixed phospholipid bilayers Biochemistry 21 1982 3487 3502
62. K.A. Riske, R.P. Barroso, C.C. Vequi-Suplicy, R. Germano, V.B. Henriques, and M.T. Lamy Lipid bilayer pre-transition as the beginning of the melting process Biochim. Biophys. Acta Biomembr. 1788 2009 954 963
63. T. Heimburg A model for the lipid pretransition: coupling of ripple formation with the chain-melting transition Biophys. J. 78 2000 1154 1165
64. 1H NMR and electronic absorption spectroscopy Physiol. Chem. Phys. Med. NMR 27 1995 1 15
65. P.M. Nassar, L.E. Almeida, and M. Tabak Binding of dipyridamole to phospholipid vesicles: a fluorescence study Biochim. Biophys. Acta 1328 1997 140 150
66. S.A. Barghouthi Thermodynamic studies of antimalarial drugs and their interaction with myoglobin, hemoglobin and phospholipid model membranes J. Appl. Sci. 5 2005 540 545
67. E. de Paula, and S. Schreier Use of a novel method for determination of partition coefficients to compare the effect of local anesthetics on membrane structure Biochim. Biophys. Acta 1240 1995 25 33
68. 13C-NMR spectroscopy J. Heterocycl. Chem. 20 1983 273 275
69. H. Satake, T. Kageyama, H. Matsuki, and S. Kaneshina Membrane-buffer partition coefficients of a local anesthetic tetracaine monitored by an anesthetic sensor; effects of temperature and pH Toxicol. Lett. 100-101 1998 441 445
70. C.P.F. Borges, I.E. Borissevitch, and M. Tabak Charge- and pH-dependent binding sites of dipyridamole in ionic micelles: a fluorescence study J. Luminesc. 65 1995 105 112
71. A. Tamura, N. Moriwaki, and T. Fujii Disturbing effect of cationic amphiphilic drugs on phospholipid asymmetry of the membrane lipid bilayer of human erythrocytes Chem. Pharm. Bull. 31 1983 1692 1697
72. L. McEvoy, P. Williamson, and R.A. Schlegel Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages Proc. Natl. Acad. Sci. U.S.A. 83 1986 3311 3315
73. J.A.F. OpdenKamp Lipid asymmetry in membranes Annu. Rev. Biochem. 48 1979 47 71
74. J.H. Williams, M. Kuchmak, and R.F. Witter Fatty acids in phospholipids isolated from human red cells Lipids 1 1966 391 398
75. L.L. Hsiao, R.J. Howard, M. Aikawa, and T.F. Taraschi Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum Biochem. J. 274 1991 121 132
76. R.L. Beaudoin, and M. Aikawa Primaquine-induced changes in morphology of exoerythrocytic stages of malaria Science 160 1968 1233 1234
77. F.L. Ginn, P. Hochstein, and B.F. Trump Membrane alterations in hemolysis: internalization of plasmalemma induced by primaquine Science 164 1969 843 845
78. R.R. Hiebsch, T.J. Raub, and B.W. Wattenberg Primaquine blocks transport by inhibiting the formation of functional transport vesicles J. Biol. Chem. 266 1991 20323 20328
79. H. Hagerstrand, T.H. Holmstrom, M. Bobrowsca-Hagerstrand, J.E. Eriksson, and B. Isomaa Amphiphile-induced phosphatidylserine exposure in human erythrocytes Mol. Membr. Biol. 15 1998 89 95
80. S. Schwarz, C.W. Haest, and B. Deuticke Extensive electroporation abolishes experimentally induced shape transformations of erythrocytes: a consequence of phospholipid symmetrization? Biochim. Biophys. Acta 1421 1999 361 379
81. H. Hagerstrand, V. Kralj-Iglic, M. Fosnaric, M. Bobrowsca-Hagerstrand, A. Wrobel, L. Mrowczynska, T. Soderstrom, and A. Iglic Endovesicle formation and membrane perturbation induced by polyoxyethyleneglycolalkylethers in human erythrocytes Biochim. Biophys. Acta Biomembr. 1665 2004 191 200
82. R. Chevli, and C.D. Fitch The antimalarial drug mefloquine binds to membrane phospholipids Antimicrob. Agents Chemother. 21 1982 581 586
83. R. Zidovetzki, I.W. Sherman, A. Atiya, and H. De Boeck A nuclear magnetic resonance study of the interactions of the antimalarials chloroquine, quinacrine, quinine and mefloquine with dipalmitoylphosphatidylcholine bilayers Mol. Biochem. Parasitol. 35 1989 199 207
84. I. Porcar, A. Codoñer, C.M. Gomez, C. Abad, and A. Campos Interaction of quinine with model lipid membranes of different compositions J. Pharm. Sci. 92 2003 45 57
85. L.Y. Lim, and M.L. Go A differential scanning calorimetry study of the interaction of the anti-malarial agent halofanthrine with dipalmitoyl phosphatidyl choline bilayers Chem. Pharm. Bull. 43 1995 2226 2231
86. G. Shalmiev, and H. Ginsburg The susceptibility of the malarial parasite Plasmodium falciparum to quinoline-containing drugs is correlated to the lipid composition of the infected erythrocyte membranes Biochem. Pharmacol. 46 1993 365 374
87. N. Vale, R. Moreira, and P. Gomes Primaquine revisited six decades after its discovery Eur. J. Med. Chem. 44 2009 937 953