Insight into NSAID-induced membrane alterations, pathogenesis and therapeutics: Characterization of interaction of NSAIDs with phosphatidylcholine

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 7, 2012, Pages 994-1002

  Lichtenberger, Lenard M ^a   Zhou, Yong ^a   Jayaraman, Vasanthi ^a   Doyen, Janice R ^a   O'Neil, Roger G ^a   Dial, Elizabeth J ^a   Volk, David E ^a   Gorenstein, David G ^a   Boggara, Mohan Babu ^b   Krishnamoorti, Ramanan ^b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

Anti inflammatory; Membrane; NSAIDs; Phospholipids; Therapeutics; Ulcer

Indexed keywords

ACETYLSALICYLIC ACID; IBUPROFEN; NAPROXEN; PHOSPHATIDYLCHOLINE;

ARTICLE; BIOMECHANICS; CARBON NUCLEAR MAGNETIC RESONANCE; CELL CULTURE; DRUG PROTEIN BINDING; DRUG STRUCTURE; GASTROINTESTINAL TOXICITY; HUMAN; HYDROPHOBICITY; IMAGING; INFRARED SPECTROSCOPY; MEMBRANE BIOLOGY; MEMBRANE FLUIDITY; MEMBRANE PERMEABILITY; MEMBRANE STABILIZATION; MOLECULAR DYNAMICS; PATHOGENESIS; PEPTIC ULCER; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SIMULATION; STOMACH HEMORRHAGE; STOMACH MUCOSA INJURY; SURFACE PLASMON RESONANCE;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPIRIN; CELL LINE, TUMOR; CELL MEMBRANE PERMEABILITY; FLUORESCENT DYES; GASTRIC MUCOSA; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IBUPROFEN; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; NAPROXEN; PHOSPHATIDYLCHOLINES; PYRIDINIUM COMPOUNDS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE PLASMON RESONANCE;

EID: 84860820855     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2012.04.002     Document Type: Article

References (84)

1. D.E. Furst, and H.E. Paulus Aspirin and Other Nonsteroidal Anti-inflammatory Drugs D.J. McCarty, W.J. Koopman, Arthritis and Allied Conditions 1993 Lea & Febiger Philadelphia 567 602
2. A.R. Chan, E.L. Giovannucci, J.A. Meyerhardt, E.S. Schernhammer, K. Wu, and C.S. Fuchs Aspirin Dose and Duration of Use and Risk of Colorectal Cancer in Men Gastroenterology 134 2008 21 28
3. A.T. Chan, S. Ogino, and C.S. Fuchs Aspirin use and survival after diagnosis of colorectal cancer JAMA 302 2009 649 658
4. B.R. Cole, R.F. Logan, S. Halabi, R. Benamouzig, R.S. Sandler, M.J. Grainge, S. Chaussade, and J.A. Baron Aspirin for the Chemoprevention of Colorectal Adenomas: Meta-analysis of the Randomized Trials J. Natl. Cancer Inst. 101 2009 256 266
5. N.R. Cook, I.M. Lee, J.M. Gaziano, D. Gordon, P.M. Ridker, J.E. Manson, C.H. Hennekens, and J.E. Buring Low-dose aspirin in the primary prevention of cancer: the Women's Health Study: a randomized controlled trial JAMA 294 2005 47 55
6. M. Etminan, S. Gill, and A. Samii Effect of non-steroidal anti-inflammatory drugs on risk of Alzheimer's disease: systematic review and meta-analysis of observational studies BMJ 327 2003 128
7. E. Flossmann, and P.M. Rothwell Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies Lancet 369 2007 1603 1613
8. P.R. Hebert, and C.H. Hennekens An overview of the 4 randomized trials of aspirin therapy in the primary prevention of vascular disease Arch. Intern. Med. 160 2000 3123 3127
9. J.-P. Pelletier Pathological Pathways of Osteoarthritis Non-steroidal Anti-imflammatory Drugs: A Research and Clinical Perspective 1994 Royal Society of Medicine Press London 1 14
10. A. Samil, M. Etiminan, M.O. Wiens, and S. Jafari NSAID Use and the Risk of Parkinson's Disease: Systematic Review and Meta-analysis of Observational Studies Drugs Aging 26 2009 769 779
11. B.A. Veld, A. Ruitenberg, and A. Hofman Nonsteroidal Anti-inflammatory Drugs and the Risk of Alzheimer's Disease N. Engl. J. Med. 345 2001 1515 1521
12. J.L. Wallace Nonsteroidal anti-inflammatory drugs and gastroenteropathy: the second hundred years Gastroenterology 112 1997 1000 1016
13. M.C. Allison, A.G. Howatson, C.J. Torrance, F.D. Lee, and R.I. Russell Gastrointestinal damage associated with the use of nonsteroidal antiinflammatory drugs N. Engl. J. Med. 327 1992 749 754
14. S.E. Gabriel, L. Jaakkimainen, and C. Bombardier Risk for serious gastrointestinal complications related to use of nonsteroidal anti-inflammatory drugs. A meta-analysis Ann. Intern. Med. 115 1991 787 796
15. C.J. Hawkey Nonsteroidal anti-inflammatory drug gastropathy Gastroenterology 119 2000 521 535
16. R.J. Flower, and J.R. Vane Inhibition of prostaglandin synthetase in brain explains the anti-pyretic activity of paracetamol (4-acetamidophenol) Nature 240 1972 410 411
17. J.A. Mitchell, P. Akarasereenont, C. Thiemermann, R.J. Flower, and J.R. Vane Selectivity of nonsteroidal antiinflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase Proc. Natl. Acad. Sci. U. S. A. 90 1993 11693 11697
18. J.L. Masferrer, B.S. Zweifel, P.T. Manning, S.D. Hauser, K.M. Leahy, W.G. Smith, P.C. Isakson, and K. Seibert Selective inhibition of inducible cyclooxygenase 2 in vivo is antiinflammatory and nonulcerogenic Proc. Natl. Acad. Sci. U. S. A. 91 1994 3228 3232
19. C. Bombardier, L. Laine, A. Reicin, D. Shapiro, R. Burgos-Vargas, B. Davis, R. Day, M.B. Ferraz, C.J. Hawkey, M.C. Hochberg, T.K. Kvien, and T.J. Schnitzer Comparison of upper gastrointestinal toxicity of rofecoxib and naproxen in patients with rheumatoid arthritis. VIGOR Study Group N. Engl. J. Med. 343 2000 1520 1528 1522 pp. following 1528
20. D. Mukherjee, S.E. Nissen, and E.J. Topol Risk of cardiovascular events associated with selective COX-2 inhibitors JAMA 286 2001 954 959
21. L.A. Garcia Rodriguez, A. Gonzalez-Perez, H. Bueno, and J. Hwa NSAID use selectively increases the risk of non-fatal myocardial infarction: a systematic review of randomised trials and observational studies PLoS One 6 2011 e16780
22. L.M. Lichtenberger, Z.M. Wang, J.J. Romero, C. Ulloa, J.C. Perez, M.N. Giraud, and J.C. Barreto Non-steroidal anti-inflammatory drugs (NSAIDs) associate with zwitterionic phospholipids: insight into the mechanism and reversal of NSAID-induced gastrointestinal injury Nat. Med. 1 1995 154 158
23. L.M. Lichtenberger, Z.M. Wang, M.N. Giraud, J.J. Romero, and J.C. Barreto Effect of naproxen (NAP) on gastric mucosal hydrophobicity: possible interaction with surface phospholipids Gastroenterology 10 1995 A149
24. H. Ferreira, M. Lucio, B. DeCastro, P. Gameriro, J.L.F.C. Lima, and S. Reis Partition and localization of nimesulide in EPC liposomes: a spectrophotometric and fluorescence study Anal. Bioanal. Chem. 377 2003 293 298
25. I. Kyrikou, S.K. Hadjikakou, D. Kovala-Demertzi, K. Viras, and T. Mavromoustakos Effects of non-steroid anti-inflammatory drugs in membrane bilayers Chem. Phys. Lipids 132 2004 157 169
26. L.M. Lichtenberger, E.J. Dial, V. Jayaraman, Z.H. Zhou, R. Krishnamorti, D.E. Volk, D.G. Gorenstein, and U. Marathi Evaluation of the structural properties and activities of a purified PC-NSAID preparation Gastroenterology 130 2006 A270
27. M. Lucio, F. Bringeza, S. Reis, J.L. Lima, and G. Brezinsinski Binding of nonsteroidal anti-inflammatory drugs to DPPC: structure and thermodynamic aspects Langmuir 24 2008 4132 4139
28. M.M. Moreno, P. Garidel, M. Suwalsky, J. Howe, and K. Brandenburg The membrane-activity of Ibuprofen, Diclofenac, and Naproxen: a physico-chemical study with lecithin phospholipids Biochim. Biophys. Acta 1788 2009 1296 1303
29. M.N. Giraud, C. Motta, J.J. Romero, G. Bommelaer, and L.M. Lichtenberger Interaction of indomethacin and naproxen with gastric surface-active phospholipids: a possible mechanism for the gastric toxicity of nonsteroidal anti-inflammatory drugs (NSAIDs) Biochem. Pharmacol. 57 1999 247 254
30. L.M. Lichtenberger, E.J. Dial, V. Jayaraman, Y. Zhou, R. Krishnamorti, D.E. Volk, D.G. Gorenstein, and U. Marathi Evaluation of the structural properties and activities of a purified PC-NSAID preparation Gastroenterology 130 2006 A-270
31. V. Jayaraman, S. Thiran, and D.R. Madden Fourier transform infrared spectroscopic characterization of a photolabile precursor of glutamate FEBS Lett. 475 2000 278 282
32. Y.N. Abdiche, and D.G. Myszka Probing the mechanism of drug/lipid membrane interactions using Biacore Anal. Biochem. 328 2004 233 243
33. A.A. Bothner-By, R.L. Stephens, J. Lee, C.D. Warren, and R.W. Jeanloz Structure determination of a tetrasaccharide: transient nuclear Overhauser effects in the rotating frame J. Am. Chem. Soc. 106 1984 811 813
34. L. Mueller Sensitivity enhanced detection of weak nuclei using heteronuclear multiple quantum coherence J. Am. Chem. Soc. 101 1979 4481 4484
35. D.A. Case, D.A. Pearlman, J.W. Caldwell, T.E. Cheatham III, W.S. Rose, C.L. Simmerling, K.M. Darden, R.V. Merz, A.L. Stanton, J.J. Cheng, M. Vincent, D.M. Crowley, R.J. Ferguson, G.L. Radmer, U.C. Seibel, P.K. Singh, S.J. Weiner, and P.A. Kollman AMBER6 1999 University of California San Francisco, CA
36. M.J. Frisch, G.W. Trucks, H.B. Schegel, G.E. Scuseria, J.R.M.A. Robb, V.G. Cheeseman, J.A. Zakrzewski, J. Montgomery, R.E. Stratmann, J.C. Burant, S. Dapprich, J.M. Millam, A.D. Daniels, K.N. Kudin, M.C. Strain, O. Farkas, J. Tomasi, V. Barone, M. Cossi, R. Cammi, B. Mennucci, C. Pomelli, C. Adamo, S. Clifford, J. Ochterski, G.A. Petersson, P.Y. Ayala, Q. Cui, K. Morokuma, P. Salvador, J.J. Da(30)nnenberg, D.K. Malick, A.D. Rabuck, K. Raghavachari, J.B. Foresman, J. Cioslowski, J. Cioslowski, J.V. Ortiz, A.G. Baboul, B.B. Stefanov, G. Lui, A. Liashenko, P. Piskorz, I. Komaromi, R. Gomperts, R.L. Martin, D.J. Fox, T. Keith, M.A. Al-Laham, C.Y. Peng, A. Nanayakkara, M. Challacombe, P.M.W. Gill, B.G. Johnson, W. Chen, M.W. Wong, J.L. Andres, C. Gomalez, M. Head-Gordon, E.S. Replogle, and J.A. Pople GAUSSIAN 98 (Revision A.11) 2001 Gaussian, Inc. Pittsburgh, PA
37. C.I. Bayly, P. Cieplak, W. Cornell, and P.A. Kollman A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model J. Phys. Chem. 97 1993 10269 10280
38. H.J.C. Berendsen, D. van der Spoel, and R. van Drunen GROMACS: A message-passing parallel molecular dynamics implementation Comput. Phys. Commun. 91 1995 43
39. E. Lindahl, B. Hess, and D. van der Spoel GROMACS 3.0: a package for molecular simulation and trajectory analysis J. Mol. Model. 7 2001 306 317
40. D.P. Tieleman, and H.J.C. Berendsen Molecular dynamics simulations of a fully hydrated dipalmitoylphosphatidylcholine bilayer with different macroscopic boundary conditions and parameters J. Chem. Phys. 105 1996 4871 4880
41. D.P. Tieleman http://moose.bio.ucalgary.ca/index.php?page=Structures-and- Topologies 2002
42. O. Berger, O. Edholm, and F. Jahnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
43. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, and J. Hermans Interaction models for water in relation to protein hydration, Intermolecular Forces 1981 331
44. A.W. Schuettelkopf, and D.M. van Aalten PRODRG - a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D 60 2004 1355 1363 http://davapc1.bioch.dundee.ac.uk/
45. J.P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
46. S. Miyamoto, and P.A. Kollman SETTLE: an analytical version of the SHAKE and RATTLE algorithm for rigid water models J. Comput. Chem. 13 1992
47. 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
48. 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
49. W. Humphrey, A. Dalke, and K. Schulten VMD: Visual molecular dynamics J. Mol. Graph. 14 1996 33 38
50. L.M. Lichtenberger, M. Barron, and U. Marathi Association of phosphatidylcholine and NSAIDs as a novel strategy to reduce gastrointestinal toxicity Drugs Today (Barc) 45 2009 877 890
51. R.J. Ober, and E.S. Ward The choice of reference cell in the analysis of kinetic data using BIAcore Anal. Biochem. 271 1999 70 80
52. A. Bax, and R. Freeman Investigation of complex networks of spin-spin coupling by two-dimensional NMR J. Magn. Reson. 44 1981 542 561
53. A.D. Bax, and D.G. Davis MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy J. Magn. Reson. 63 1985 207 213
54. H. Chakraborty, R. Banerjee, and M. Sarkar Incorporation of NSAIDs in micelles: implication of structural switchover in drug-membrane interaction Biophys. Chem. 104 2003 315 325
55. H. Chakraborty, S. Roy, and M. Sarkar Interaction of oxicam NSAIDs with DMPC vesicles: differential partitioning of drugs Chem. Phys. Lipids 138 2005 20 28
56. K. Vanommeslaeghe, E. Hatcher, C. Acharya, S. Kundu, S. Zhong, J. Shim, E. Darian, O. Guvench, P. Lopes, I. Vorobyov, and A.D. Mackerell Jr. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 31 2010 691-690
57. M.B. Boggara Lipid-based drug delivery system - molecular dynamics simulations and neutron scattering studies Chemical and Biomolecular Engineering 2009 University of Houston Houston, USA 238 vol. PhD
58. M.B. Boggara, and R. Krishnamoorti Partitioning of nonsteroidal antiinflammatory drugs in lipid membranes: a molecular dynamics simulation study Biophys. J. 98 2010 586 595
59. R.J. Clarke Effect of lipid structure on the dipole potential of phosphatidylcholine bilayers Biochim. Biophys. Acta 1327 1997 269 278
60. R.J. Clarke The dipole potential of phospholipid membranes and methods for its detection Adv. Colloid Interface Sci. 89-90 2001 263 281
61. T. Starke-Peterkovic, N. Turner, M.F. Vitha, M.P. Waller, D.E. Hibbs, and R.J. Clarke Cholesterol effect on the dipole potential of lipid membranes Biophys. J. 90 2006 4060 4070
62. T. Starke-Peterkovic, and R.J. Clarke Effect of headgroup on the dipole potential of phospholipid vesicles Eur. Biophys. J. 39 2009 103 110
63. Y. Zhou, R. Doyen, and L.M. Lichtenberger The role of membrane cholesterol in determining bile acid cytotoxicity and cytoprotection of ursodeoxycholic acid Biochim. Biophys. Acta 1788 2009 507 513
64. J.L. Williams, N. Nath, J. Chen, T.R. Hundley, J. Gao, L. Kopelovich, K. Kashfi, and B. Rigas Growth inhibition of human colon cancer cells by nitric oxide (NO)-donating aspirin is associated with cyclooxygenase-2 induction and beta-catenin/T-cell factor signaling, nuclear factor-kappaB, and NO synthase 2 inhibition: implications for chemoprevention Cancer Res. 63 2003 7613 7618
65. M. Tsujii, S. Kawano, S. Tsuji, H. Sawaoka, M. Hori, and R.N. DuBois Cyclooxygenase regulates angiogenesis induced by colon cancer cells Cell 93 1998 705 716
66. J.R. Vane, and R.M. Botting Control of the circulation by vasoactive mediators from endothelial cells J. Lipid Mediat. Cell Signal. 9 1994 1 8
67. P.J. Goddard, B.A. Hills, and L.M. Lichtenberger Does aspirin damage canine gastric mucosa by reducing its surface hydrophobicity? Am. J. Physiol. 252 1987 G421 G430
68. P.J. Goddard, Y.C. Kao, and L.M. Lichtenberger Luminal surface hydrophobicity of canine gastric mucosa is dependent on a surface mucous gel Gastroenterology 98 1990 361 370
69. L.M. Lichtenberger The hydrophobic barrier properties of gastrointestinal mucus Annu. Rev. Physiol. 57 1995 565 583
70. J. Husch, B. Dutagaci, C. Glaubitz, T. Geppert, G. Schneider, M. Harms, C.C. Muller-Goymann, L. Fink, M.U. Schmidt, C. Setzer, J. Zirkel, H. Rebmann, M. Schubert-Zsilavecz, and LM. Abdel-Tawab Structural properties of so-called NSAID-phospholipid-complexes Eur. J. Pharm. Sci. 44 2011 103 116
71. B.A. Hills, B.D. Butler, and L.M. Lichtenberger Gastric mucosal barrier: hydrophobic lining to the lumen of the stomach Am. J. Physiol. 244 1983 G561 G568
72. F.L. Lanza, U.K. Marathi, B.S. Anand, and L.M. Lichtenberger Clinical trial: comparison of ibuprofen-phosphatidylcholine and ibuprofen on the gastrointestinal safety and analgesic efficacy in osteoarthritic patients Aliment. Pharmacol. Ther. 28 2008 431 442
73. Y. Zhou, and R.M. Raphael Effect of salicylate on the elasticity, bending stiffness, and strength of SOPC membranes Biophys. J. 89 2005 1789 1801
74. M.B. Boggara, A. Faraone, and R. Krishnamoorti Effect of pH and ibuprofen on the phospholipid bilayer bending modulus J. Phys. Chem. B 114 2010 8061 8066
75. L.M. Lichtenberger, Y. Zhou, E.J. Dial, and R.M. Raphael NSAID injury to the gastrointestinal tract: evidence that NSAIDs interact with phospholipids to weaken the hydrophobic surface barrier and induce the formation of unstable pores in membranes J. Pharm. Pharmacol. 58 2006 1421 1428
76. C. Nunes, G. Brezesinski, J.L. Lima, S. Reis, and M. Lucio Synchrotron SAXS and WAXS study of the interactions of NSAIDs with lipid membranes J. Phys. Chem. B 115 2011 8024 8032
77. C. Nunes, G. Brezesinski, C. Pereira-Leite, J.L. Lima, S. Reis, and M. Lucio NSAIDs interactions with membranes: a biophysical approach Langmuir 27 2011 10847 10858
78. M.B. Boggara, and R. Krishnamoorti Small-angle neutron scattering studies of phospholipid-NSAID adducts Langmuir 26 2010 5734 5745
79. M.B. Boggara, R. Krishnamoorti, Partitioning of nonsteroidal antiinflammatory drugs in lipid membranes: a molecular dynamics simulation study, Biophys J 98 586-595.
80. L.M. Lichtenberger, J.J. Romero, E.J. Dial, and J.E. Moore Naproxen-PC: A GI Safe and Highly Effective Anti-inflammatory Inflammopharmacology 16 2008 1 5
81. B.S. Anand, J.J. Romero, S.K. Sanduja, and L.M. Lichtenberger Phospholipid association reduces the gastric mucosal toxicity of aspirin in human subjects Am. J. Gastroenterol. 94 1999 1818 1822
82. B. Cryer, D.L. Bhatt, F.L. Lanza, J.F. Dong, L.M. Lichtenberger, and U.K. Marathi Low-Dose Aspirin-Induced Ulceration Is Attenuated by Aspirin-Phosphatidylcholine: A Randomized Clinical Trial Am. J. Gastroenterol. 106 2011 272 277
83. Y. Zhou, J.F. Hancock, and L.M. Lichtenberger The nonsteroidal anti-inflammatory drug indomethacin induces heterogeneity in lipid membranes: potential implication for its diverse biological action PLoS One 5 2010 e8811
84. Y. Zhou, S.J. Plowman, L.M. Lichtenberger, and J.F. Hancock The anti-inflammatory drug indomethacin alters nanoclustering in synthetic and cell plasma membranes J. Biol. Chem. 285 2010 35188 35195