Reinforcing the membrane-mediated mechanism of action of the anti-tuberculosis candidate drug thioridazine with molecular simulations

Journal of Computer-Aided Molecular Design

Volumn 28, Issue 2, 2014, Pages 123-134

  Kopec, Wojciech ^a   Khandelia, Himanshu ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Antipsychotics; Drug membrane interactions; Lipid bilayer; M. tuberculosis; Molecular dynamics

Indexed keywords

CYTOLOGY; DRUG INTERACTIONS; DRUG THERAPY; INSECTICIDES; LIPID BILAYERS;

ANTIPSYCHOTIC; CANDIDATE DRUGS; DOPAMINE; DRUG-MEMBRANE INTERACTION; M. TUBERCULOSIS; MECHANISM OF ACTION; MEMBRANE INTERACTIONS; MOLECULAR SIMULATIONS; NEGATIVELY CHARGED; THIORIDAZINE;

MOLECULAR DYNAMICS;

AMPHOLYTE; THIORIDAZINE; LIPID BILAYER; TUBERCULOSTATIC AGENT;

ARTICLE; DRUG MECHANISM; HYDROGEN BOND; LIPID BILAYER; LIPID MEMBRANE; MICELLE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; STATIC ELECTRICITY; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS;

ANTITUBERCULAR AGENTS; CELL MEMBRANE; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; THIORIDAZINE;

EID: 84898823299     PISSN: 0920654X     EISSN: 15734951     Source Type: Journal    
DOI: 10.1007/s10822-014-9737-z     Document Type: Article

References (78)

1. Schreier S, Malheiros SV, de Paula E (2000) Surface active drugs: self-association and interaction with membranes and surfactants. Physicochemical and biological aspects. Biochim Biophys Acta 1508(1-2):210-234
2. Imming P, Sinning C, Meyer A (2006) Drugs, their targets and the nature and number of drug targets. Nat Rev Drug Discov 5(10):821-834 (Pubitemid 44480536)
3. Hendrich AB, Michalak K (2003) Lipids as a target for drugs modulating multidrug resistance of cancer cells. Curr Drug Targets 4(1):23-30 (Pubitemid 36131638)
4. Khandelia H, Ipsen JH, Mouritsen OG (2008) The impact of peptides on lipid membranes. Biochim Biophys Acta Biomembr 1778(7-8):1528-1536
5. Jutila A, Söderlund T, Pakkanen AL, Huttunen M, Kinnunen PKJ (2001) Comparison of the effects of clozapine, chlorpromazine, and haloperidol on membrane lateral heterogeneity. Chem Phys Lipids 112(2):151-163 (Pubitemid 32817150)
6. Killian JA (1998) Hydrophobic mismatch between proteins and lipids in membranes. Biochim Biophys Acta Rev Biomembr 1376(3):401-415
7. Jensen MØ, Mouritsen OG (2004) Lipids do influence protein function - the hydrophobic matching hypothesis revisited. Biochim Biophys Acta Biomembr 1666(1-2):205-226 (Pubitemid 39429479)
8. Cantor RS (1997) The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry 36(9):2339-2344
9. Cantor RS (1997) Lateral pressures in cell membranes: a mechanism for modulation of protein function. J Phys Chem B 101(10):1723-1725
10. Kopec W, Telenius J, Khandelia H (2013) Molecular dynamics simulations of the interactions of medicinal plant extracts and drugs with lipid bilayer membranes. FEBS J. doi:10.1111/febs.12286
11. Seeger HM, Gudmundsson ML, Heimburg T (2007) How anesthetics, neurotransmitters, and antibiotics influence the relaxation processes in lipid membranes. J Phys Chem B 111(49):13858-13866
12. Scheidt HA, Huster D (2008) The interaction of small molecules with phospholipid membranes studied by 1H NOESY NMR under magic-angle spinning. Acta Pharmacol Sin 29(1):35-49
13. Barry J, Fritz M, Brender JR, Smith PES, Lee D-K, Ramamoorthy A (2009) 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(12):4490-4498. doi:10.1021/ja809217u
14. Klitgaard JK, Skov MN, Kallipolitis BH, Kolmos HJ (2008) Reversal of methicillin resistance in Staphylococcus aureus by thioridazine. J Antimicrob Chemother 62(6):1215-1221
15. Thanacoody HK (2007) Thioridazine: resurrection as an antimicrobial agent? Br J Clin Pharmacol 64(5):566-574. doi:10.1111/j.1365-2125.2007.03021.x
16. Abbate E, Vescovo M, Natiello M, Cufre M, Garcia A, Gonzalez Montaner P, Ambroggi M, Ritacco V, van Soolingen D (2012) Successful alternative treatment of extensively drug-resistant tuberculosis in Argentina with a combination of linezolid, moxifloxacin and thioridazine. J Antimicrob Chemother 67(2):473-477. doi:10.1093/jac/dkr500
17. Lialiaris T, Pantazaki A, Sivridis E, Mourelatos D (1992) Chlorpromazine-induced damage on nucleic acids: a combined cytogenetic and biochemical study. Mutat Res Fundam Mol Mech Mutagen 265(2):155-163
18. Sharma S, Singh A (2011) Phenothiazines as anti-tubercular agents: mechanistic insights and clinical implications. Expert Opin Invest Drugs 20(12):1665-1676
19. Salih FA, Kaushik NK, Sharma P, Choudary GV, Murthy PS, Venkitasubramanian TA (1991) Calmodulin-like activity in mycobacteria. Indian J Biochem Biophys 28(5-6):491-495
20. Michalak K, Wesolowska O, Motohashi N, Molnar J, Hendrich AB (2006) Interactions of phenothiazines with lipid bilayer and their role in multidrug resistance reversal. Curr Drug Targets 7(9):1095-1105 (Pubitemid 44356009)
21. Langerman L, Bansinath M, Grant GJ (1994) The partition coefficient as a predictor of local anesthetic potency for spinal anesthesia: evaluation of five local anesthetics in a mouse model. Anesth Analg 79(3):490-494 (Pubitemid 24279847)
22. Forrest FM, Forrest IS, Roizin L (1963) Clinical, biochemical and post mortem studies on a patient treated with chlorpromazine. Agressologie 4:259-265
23. Sachlos E, Risueno RM, Laronde S, Shapovalova Z, Lee JH, Russell J, Malig M, McNicol JD, Fiebig-Comyn A, Graham M, Levadoux-Martin M, Lee JB, Giacomelli AO, Hassell JA, Fischer-Russell D, Trus MR, Foley R, Leber B, Xenocostas A, Brown ED, Collins TJ, Bhatia M (2012) Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 149(6):1284-1297. doi:10.1016/j.cell.2012.03.049
24. Seeman P, Lee T (1975) Antipsychotic drugs: direct correlation between clinical potency and presynaptic action on dopamine neurons. Science 188(4194):1217-1219
25. Carlo RD, Muccioli G, Bellussi G, Portaleone P, Ghi P, Racca S, Carlo FD (1986) Steroid, prolactin, and dopamine receptors in normal and pathologic breast tissue. Ann NY Acad Sci 464(1):559-562. doi:10.1111/j.1749-6632.1986. tb16068.x (Pubitemid 17197695)
26. Peters GH, Wang C, Cruys-Bagger N, Velardez GF, Madsen JJ, Westh P (2013) Binding of serotonin to lipid membranes. J Am Chem Soc 135(6):2164-2171. doi:10.1021/ja306681d
27. Jodko-Piorecka K, Litwinienko G (2013) First experimental evidence of dopamine interactions with negatively charged model biomembranes. ACS Chem Neurosci. doi:10.1021/cn4000633
28. Orlowski A, Grzybek M, Bunker A, Pasenkiewicz-Gierula M, Vattulainen I, Mannisto PT, Rog T (2012) Strong preferences of dopamine and l-dopa towards lipid head group: importance of lipid composition and implication for neurotransmitter metabolism. J Neurochem 122(4):681-690. doi:10.1111/j.1471- 4159.2012.07813.x
29. Amaral L, Kristiansen JE, Viveiros M, Atouguia J (2001) Activity of phenothiazines against antibiotic-resistant Mycobacterium tuberculosis: a review supporting further studies that may elucidate the potential use of thioridazine as anti-tuberculosis therapy. J Antimicrob Chemother 47(5):505-511
30. Castaing M, Brouant P, Loiseau A, Santelli-Rouvier C, Santelli M, Alibert-Franco S, Mahamoud A, Barbe J (2000) Membrane permeation by multidrug-resistance-modulators and non-modulators: effects of hydrophobicity and electric charge. J Pharm Pharmacol 52(3):289-296 (Pubitemid 30189383)
31. Gulyaeva N, Zaslavsky A, Lechner P, Chlenov M, McConnell O, Chait A, Kipnis V, Zaslavsky B (2003) Relative hydrophobicity and lipophilicity of drugs measured by aqueous two-phase partitioning, octanol-buffer partitioning and HPLC. A simple model for predicting blood-brain distribution. Eur J Med Chem 38(4):391-396 (Pubitemid 36577189)
32. Christensen JB, Hendricks O, Chaki S, Mukherjee S, Das A, Pal TK, Dastidar SG, Kristiansen JE (2013) A comparative analysis of in vitro and in vivo efficacies of the enantiomers of thioridazine and its racemate. PLoS One 8(3):e57493. doi:10.1371/journal.pone.0057493
33. Berger O, Edholm O, Jahnig F (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72(5):2002-2013. doi:10.1016/s0006-3495(97)78845-3 (Pubitemid 27184429)
34. Bachar M, Brunelle P, Tieleman DP, Rauk A (2004) Molecular dynamics simulation of a polyunsaturated lipid bilayer susceptible to lipid peroxidation. J Phys Chem B 108(22):7170-7179. doi:10.1021/Jp036981u
35. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J (1981) Interaction models for water in relation to protein hydration. Intermolecular Forces 14:331-342
36. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA Jr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Laham A, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA (2004) Gaussian 03. Gaussian, Inc., Wallingford, CT
37. Van Gunsteren WF, Berendsen HJC (1987) Groningen molecular simulation (GROMOS). Library manual, Biomos, Groningen, The Netherlands, p 1-221
38. van Buuren AR, Marrink SJ, Berendsen HJC (1993) A molecular dynamics study of the decane/water interface. J Phys Chem 97(36):9206-9212. doi:10.1021/j100138a023
39. Mark AE, van Helden SP, Smith PE, Janssen LHM, van Gunsteren WF (1994) Convergence properties of free energy calculations: alpha.-cyclodextrin complexes as a case study. J Am Chem Soc 116(14):6293-6302. doi:10.1021/ ja00093a032 (Pubitemid 24981278)
40. Khandelia H, Witzke S, Mouritsen OG (2010) Interaction of salicylate and a terpenoid plant extract with model membranes: reconciling experiments and simulations. Biophys J 99(12):3887-3894. doi:10.1016/j.bpj.2010.11.009
41. Lindahl E, Hess B, van der Spoel D (2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 7(8):306-317 (Pubitemid 36153547)
42. Leach AR (2001) Molecular modeling principles and applications, 2nd edn. Pearson Education Limited, p 356
43. Hess B (2008) P-LINCS: a parallel linear constraint solver for molecular simulation. J Chem Theory Comput 4(1):116-122
44. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J Chem Phys 98(12):10089-10092
45. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103(19):8577-8593
46. Berendsen HJC, Postma JPM, Van Gunsteren WF, Dinola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81(8):3684-3690
47. Lindahl E, Edholm O (2000) Spatial and energetic-entropic decomposition of surface tension in lipid bilayers from molecular dynamics simulations. J Chem Phys 113(9):3882-3893
48. Irving JH, Kirkwood JG (1950) The statistical mechanical theory of transport processes. IV. The equations of hydrodynamics. J Chem Phys 18(6):817-829
49. Terama E, Ollila OHS, Salonen E, Rowat AC, Trandum C, Westh P, Patra M, Karttunen M, Vattulainen I (2008) Influence of ethanol on lipid membranes: from lateral pressure profiles to dynamics and partitioning. J Phys Chem B 112(13):4131-4139
50. Jerabek H, Pabst G, Rappolt M, Stockner T (2010) Membrane-mediated effect on ion channels induced by the anesthetic drug ketamine. J Am Chem Soc 132(23):7990-7997. doi:10.1021/ja910843d
51. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14(1):33-38 (Pubitemid 26152973)
52. Marrink SJ, Berendsen HJC (1996) Permeation process of small molecules across lipid membranes studied by molecular dynamics simulations. J Phys Chem 100(41):16729-16738 (Pubitemid 126788021)
53. Pautot S, Frisken BJ, Weitz DA (2003) Engineering asymmetric vesicles. Proc Natl Acad Sci USA 100(19):10718-10721. doi:10.1073/pnas.1931005100 (Pubitemid 37140094)
54. Abu-Baker S, Qi X, Lorigan GA (2007) Investigating the interaction of Saposin C with POPS and POPC phospholipids: a solid-state NMR spectroscopic study. Biophys J 93(10):3480-3490 (Pubitemid 350190811)
55. Mukhopadhyay P, Monticelli L, Tieleman DP (2004) Molecular dynamics simulation of a palmitoyl-oleoyl phosphatidylserine bilayerwith Na+ counterions and NaCl. Biophys J 86(3):1601-1609 (Pubitemid 38295593)
56. Ferreira TM, Coreta-Gomes F, Samuli Ollila OH, Moreno MJ, Vaz WLC, Topgaard D (2013) Cholesterol and POPC segmental order parameters in lipid membranes: solid state 1H-13C NMR and MD simulation studies. Phys Chem Chem Phys 15(6):1976-1989
57. Bagatolli LA, Ipsen JH, Simonsen AC, Mouritsen OG (2010) An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. Prog Lipid Res 49(4):378-389
58. Bagatolli LA, Mouritsen OG (2013) Is the fluid mosaic (and the accompanying raft hypothesis) a suitable model to describe fundamental features of biological membranes? What may be missing? Front Plant Sci 4:457. doi:10.3389/fpls.2013.00457
59. Cournia Z, Ullmann GM, Smith JC (2007) Differential effects of cholesterol, ergosterol and lanosterol on a dipalmitoyl phosphatidylcholine membrane: a molecular dynamics simulation study. J Phys Chem B 111(7):1786-1801 (Pubitemid 46384272)
60. Epand RM, Epand RF (2011) Bacterial membrane lipids in the action of antimicrobial agents. J Pept Sci 17(5):298-305. doi:10.1002/psc.1319
61. Riedl S, Rinner B, Asslaber M, Schaider H, Walzer S, Novak A, Lohner K, Zweytick D (2011) In search of a novel target - phosphatidylserine exposed by non-apoptotic tumor cells and metastases of malignancies with poor treatment efficacy. Biochim Biophys Acta 1808(11):2638-2645. doi:10.1016/j.bbamem.2011.07. 026
62. Milutinovic PS, Yang L, Cantor RS, Eger EI II, Sonner JM (2007) Anesthetic-like modulation of a gamma-aminobutyric acid type A, strychnine-sensitive glycine, and N-methyl-d-aspartate receptors by coreleased neurotransmitters. Anesth Analg 105(2):386-392. doi:10.1213/01.ane.0000267258. 17197.7d (Pubitemid 47196417)
63. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112-124. doi:10.1038/nrm2330 (Pubitemid 351158912)
64. Denisov G, Wanaski S, Luan P, Glaser M, McLaughlin S (1998) Binding of basic peptides to membranes produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: an electrostatic model and experimental results. Biophys J 74(2 Pt 1):731-744. doi:10.1016/s0006-3495(98)73998-0 (Pubitemid 28345268)
65. Leventis PA, Grinstein S (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407-427. doi:10.1146/annurev.biophys.093008.131234
66. Witzke S, Duelund L, Kongsted J, Petersen M, Mouritsen OG, Khandelia H (2010) Inclusion of terpenoid plant extracts in lipid bilayers investigated by molecular dynamics simulations. J Phys Chem B 114(48):15825-15831
67. Frenzel J, Arnold K, Nuhn P (1978) Calorimetric, 13C NMR, and 31P NMR studies on the interaction of some phenothiazine derivatives with dipalmitoyl phosphatidylcholine model membranes. Biochim Biophys Acta Biomembr 507(2):185-197 (Pubitemid 8267419)
68. Lichtenberger LM, Zhou Y, Jayaraman V, Doyen JR, O'Neil RG, Dial EJ, Volk DE, Gorenstein DG, Boggara MB, Krishnamoorti R (2012) Insight into NSAID-induced membrane alterations, pathogenesis and therapeutics: characterization of interaction of NSAIDs with phosphatidylcholine. Biochim Biophys Acta 1821(7):994-1002. doi:10.1016/j.bbalip.2012.04.002
69. Parry MJ, Alakoskela JMI, Khandelia H, Kumar SA, Jäättelä M, Mahalka AK, Kinnunen PKJ (2008) High-affinity small molecule-phospholipid complex formation: binding of siramesine to phosphatidic acid. J Am Chem Soc 130(39):12953-12960
70. MacCallum JL, Tieleman DP (2008) Interactions between small molecules and lipid bilayers. Curr Top Membr 60:227-256. doi:10.1016/S1063-5823(08)00008-2
71. Rog T, Pasenkiewicz-Gierula M, Vattulainen I, Karttunen M (2009) Ordering effects of cholesterol and its analogues. Biochim Biophys Acta 1788(1):97-121. doi:10.1016/j.bbamem.2008.08.022
72. Edholm O, Nagle JF (2005) Areas of molecules in membranes consisting of mixtures. Biophys J 89(3):1827-1832. doi:10.1529/biophysj.105.064329 (Pubitemid 41233537)
73. Hermetter A, Kopec W, Khandelia H (2013) Conformations of double-headed, triple-tailed phospholipid oxidation lipid products in model membranes. Biochim Biophys Acta 1828:1700-1706. doi:10.1016/j.bbamem.2013.03.030
74. Hendrich AB, Wesołowska O, Komorowska M, Motohashi N, Michalak K (2002) The alterations of lipid bilayer fluidity induced by newly synthesized phenothiazine derivative. Biophys Chem 98(3):275-285 (Pubitemid 34786440)
75. Dobrzynska I, Szachowicz-Petelska B, Sulkowski S, Figaszewski Z (2005) Changes in electric charge and phospholipids composition in human colorectal cancer cells. Mol Cell Biochem 276(1-2):113-119. doi:10.1007/s11010-005-3557-3 (Pubitemid 41236216)
76. Cantor RS (2003) Receptor desensitization by neurotransmitters in membranes: are neurotransmitters the endogenous anesthetics? Biochemistry 42(41):11891-11897
77. Samuli Ollila OH, Rog T, Karttunen M, Vattulainen I (2007) Role of sterol type on lateral pressure profiles of lipid membranes affecting membrane protein functionality: comparison between cholesterol, desmosterol, 7-dehydrocholesterol and ketosterol. J Struct Biol 159(2):311-323. doi:10.1016/j.jsb.2007.01.012 (Pubitemid 47095396)
78. Lau AY, Roux B (2007) The free energy landscapes governing conformational changes in a glutamate receptor ligand-binding domain. Structure 15(10):1203-1214. doi:10.1016/j.str.2007.07.015 (Pubitemid 47542487)