Experimental and computational studies investigating trehalose protection of HepG2 cells from palmitate-induced toxicity

Biophysical Journal

Volumn 94, Issue 7, 2008, Pages 2869-2883

  Leekumjorn, Sukit ^a   Wu, Yifei ^b   Sum, Amadeu K ^a   Chan, Christina ^b  

^a State University   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PALMITIC ACID; TREHALOSE;

ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE; CELL PROTECTION; CELL SURVIVAL; COMPUTER SIMULATION; DRUG EFFECT; HUMAN; LIVER TUMOR; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MEMBRANE; CELL SURVIVAL; COMPUTER SIMULATION; CYTOPROTECTION; HUMANS; LIVER NEOPLASMS; MODELS, BIOLOGICAL; PALMITIC ACID; TREHALOSE;

EID: 41649087624     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.120717     Document Type: Article

References (109)

1. Clandinin, M. T., S. Cheema, C. J. Field, M. L. Garg, J. Venkatraman, and T. R. Clandinin. 1991. Dietary fat: exogenous determination of membrane structure and cell function. FASEB J. 5:2761-2769.
2. Galli, C., and F. Marangoni. 1997. Recent advances in the biology of n-6 fatty acids. Nutrition. 13:978-985.
3. Yamashita, A., T. Sugiura, and K. Waku. 1997. Acyltransferases and transacylases involved in fatty acid remodeling of phospholipids and metabolism of bioactive lipids in mammalian cells. J. Biochem. (Tokyo). 122:1-16.
4. Andrade, L. N., T. M. de Lima, R. Curi, and A. M. Castrucci. 2005. Toxicity of fatty acids on murine and human melanoma cell lines. Toxicol. In Vitro. 19:553-560.
5. Lima, T. M., C. C. Kanunfre, C. Pompeia, R. Verlengia, and R. Curi. 2002. Ranking the toxicity of fatty acids on Jurkat and Raji cells by flow cytometric analysis. Toxicol. In Vitro. 16:741-747.
6. Maedler, K., G. A. Spinas, D. Dyntar, W. Moritz, N. Kaiser, and M. Y. Donath. 2001. Distinct effects of saturated and monounsaturated fatty acids on β-cell turnover and function. Diabetes. 50:69-76.
7. El-Assaad, W., J. Buteau, M. L. Peyot, C. Nolan, R. Roduit, S. Hardy, E. Joly, G. Dbaibo, L. Rosenberg, and M. Prentki. 2003. Saturated fatty acids synergize with elevated glucose to cause pancreatic β-cell death. Endocrinology. 144:4154-4163.
8. Kong, J. Y., and S. W. Rabkin. 2000. Palmitate-induced apoptosis in cardiomyocytes is mediated through alterations in mitochondria: prevention by cyclosporin A. Biochim. Biophys. Acta Mol. Cell Biol. L. 1485:45-55.
9. Sparagna, G. C., D. L. Hickson-Bick, L. M. Buja, and J. B. McMillin. 2000. A metabolic role for mitochondria in palmitate-induced cardiac myocyte apoptosis. Am. J. Physiol. Heart C. 279:H2124-H2132.
10. Dashti, N., Q. Feng, and F. A. Franklin. 2000. Long-term effects of cis and trans monounsaturated (18:1) and saturated (16:0) fatty acids on the synthesis and secretion of apolipoprotein A-I- and apolipoprotein B-containing lipoproteins in HepG2 cells. J. Lipid Res. 41:1980-1990.
11. Ji, J., L. Zhang, P. Wang, Y. M. Mu, X. Y. Zhu, Y. Y. Wu, H. Yu, B. Zhang, S. M. Chen, and X. Z. Sun. 2005. Saturated free fatty acid, palmitic acid, induces apoptosis in fetal hepatocytes in culture. Exp. Toxicol. Pathol. 56:369-376.
12. Srivastava, S., and C. Chan. 2007. Hydrogen peroxide and hydroxyl radicals mediate palmitate-induced cytotoxicity to hepatoma cells: relation to mitochondrial permeability transition. Free Radic. Res. 41:38-49.
13. Listenberger, L. L., X. Han, S. E. Lewis, S. Cases, R. V. Farese, Jr., D. S. Ory, and J. E. Schaffer. 2003. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. USA. 100:3077-3082.
14. Dobrzyn, A., and J. M. Ntambi. 2005. The role of stearoyl-CoA desaturase in the control of metabolism. Prostaglandins Leukot. Essent. Fatty Acids. 73:35-41.
15. Borradaile, N. M., X. Han, J. D. Harp, S. E. Gale, D. S. Ory, and J. E. Schaffer. 2006. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 47:2726-2737.
16. Alexander, J. J., A. Snyder, and J. H. Tonsgard. 1998. Omega-oxidation of monocarboxylic acids in rat brain. Neurochem. Res. 23:227-233.
17. Sanders, R. J., R. Ofman, F. Valianpour, S. Kemp, and R. J. Wanders. 2005. Evidence for two enzymatic pathways for ω-oxidation of dodecanoic acid in rat liver microsomes. J. Lipid Res. 46:1001-1008.
18. Listenberger, L. L., D. S. Ory, and J. E. Schaffer. 2001. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J. Biol. Chem. 276:14890-14895.
19. Lu, Z.-H., Y.-M. Mu, B.-A. Wang, X.-L. Li, J.-M. Lu, J.-Y. Li, C.-Y. Pan, T. Yanase, and H. Nawata. 2003. Saturated free fatty acids, palmitic acid and stearic acid, induce apoptosis by stimulation of ceramide generation in rat testicular Leydig cell. Biochem. Biophys. Res. Commun. 303:1002-1007.
20. Goodman, D. S. 1958. The interaction of human erythrocytes with sodium palmitate. J. Clin. Invest. 37:1729-1735.
21. Spector, A. A. 1975. Fatty acid binding to plasma albumin. J. Lipid Res. 16:165-179.
22. Pande, S. V., and J. F. Mead. 1968. Inhibition of enzyme activities by free fatty acids. J. Biol. Chem. 243:6180-6185.
23. Reaven, P., S. Parthasarathy, B. J. Grasse, E. Miller, F. Almazan, F. H. Mattson, J. C. Khoo, D. Steinberg, and J. L. Witztum. 1991. Feasibility of using an oleate-rich diet to reduce the susceptibility of low-density lipoprotein to oxidative modification in humans. Am. J. Clin. Nutr. 54:701-706.
24. Hart, C. M., M. P. Gupta, and V. Evanoff. 1997. Oleic acid reduces oxidant stress in cultured pulmonary artery endothelial cells. Exp. Lung Res. 23:405-425.
25. Toborek, M., Y. W. Lee, R. Garrido, S. Kaiser, and B. Hennig. 2002. Unsaturated fatty acids selectively induce an inflammatory environment in human endothelial cells. Am. J. Clin. Nutr. 75:119-125.
26. Li, Z., S. Srivastava, S. Mittal, X. Yang, L. Sheng, and C. Chan. 2007. A three stage integrative pathway search (TIPS) framework to identify toxicity relevant genes and pathways. BMC Bioinformatics. 8:202.
27. Kinter, M., D. R. Spitz, and R. J. Roberts. 1996. Oleic acid incorporation protects cultured hamster fibroblasts from oxygen-induced cytotoxicity. J. Nutr. 126:2952-2959.
28. Natali, F., L. Siculella, S. Salvati, and G. V. Gnoni. 2007. Oleic acid is a potent inhibitor of fatty acid and cholesterol synthesis in c6 glioma cells. J. Lipid Res. 48:1966-1975.
29. Crowe, J. H., L. M. Crowe, and S. A. Jackson. 1983. Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum. Arch. Biochem. Biophys. 220:477-484.
30. Crowe, J. H., L. M. Crowe, and D. Chapman. 1984. Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science. 223:701-703.
31. Leslie, S. B., E. Israeli, B. Lighthart, J. H. Crowe, and L. M. Crowe. 1995. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl. Environ. Microbiol. 61:3592-3597.
32. Wolkers, W. F., N. J. Walker, F. Tablin, and J. H. Crowe. 2001. Human platelets loaded with trehalose survive freeze-drying. Cryobiology. 42:79-87.
33. Elbein, A. D., Y. T. Pan, I. Pastuszak, and D. Carroll. 2003. New insights on trehalose: a multifunctional molecule. Glycobiology. 13:17r-27r.
34. Chen, Q., and G. G. Haddad. 2004. Role of trehalose phosphate synthase and trehalose during hypoxia: from flies to mammals. J. Exp. Biol. 207:3125-3129.
35. Oku, K., M. Kurose, M. Kubota, S. Fukuda, M. Kurimoto, Y. Tujisaka, A. Okabe, and M. Sakurai. 2005. Combined NMR and quantum chemical studies on the interaction between trehalose and dienes relevant to the antioxidant function of trehalose. J. Phys. Chem. B. 109:3032-3040.
36. Herdeiro, R. S., M. D. Pereira, A. D. Panek, and E. C. A. Eleutherio. 2006. Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim. Biophys. Acta Gen. Subj. 1760:340-346.
37. Benaroudj, N., D. H. Lee, and A. L. Goldberg. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276:24261-24267.
38. Cirelli, N., P. Lebrun, C. Gueuning, J. Delogne-Desnoeck, A.-M. Vanbellinghen, G. Graff, and S. Meuris. 2001. Physiological concentrations of albumin stimulate chorionic gonadotrophin and placental lactogen release from human term placental explants. Hum. Reprod. 16:441-448.
39. Boden, G., X. Chen, E. Capulong, and M. Mozzoli. 2001. Effects of free fatty acids on gluconeogenesis and autoregulation of glucose production in type 2 diabetes. Diabetes. 50:810-816.
40. Mensink, M., E. E. Blaak, M. A. van Baak, A. J. Wagenmakers, and W. H. Saris. 2001. Plasma free fatty acid uptake and oxidation are already diminished in subjects at high risk for developing type 2 diabetes. Diabetes. 50:2548-2554.
41. Skowronski, R., C. B. Hollenbeck, B. B. Varasteh, Y. D. Chen, and G. M. Reaven. 1991. Regulation of non-esterified fatty acid and glycerol concentration by insulin in normal individuals and patients with type 2 diabetes. Diabet. Med. 8:330-333.
42. Woerle, H. J., E. Popa, J. Dostou, S. Welle, J. Gerich, and C. Meyer. 2002. Exogenous insulin replacement in type 2 diabetes reverses excessive hepatic glucose release, but not excessive renal glucose release and impaired free fatty acid clearance. Metabolism. 51:1494-1500.
43. Haak, R. A., L. M. Ingraham, R. L. Baehner, and L. A. Boxer. 1979. Membrane fluidity in human and mouse Chediak-Higashi leukocytes. J. Clin. Invest. 64:138-144.
44. Squier, T. C., D. J. Bigelow, and D. D. Thomas. 1988. Lipid fluidity directly modulates the overall protein rotational mobility of the Ca-ATPase in sarcoplasmic reticulum. J. Biol. Chem. 263:9178-9186.
45. Tsuda, K., Y. Kinoshita, K. Kimura, I. Nishio, and Y. Masuyama. 2001. Electron paramagnetic resonance investigation on modulatory effect of 17β-estradiol on membrane fluidity of erythrocytes in postmenopausal women. Arterioscler. Thromb. Vasc. Biol. 21:1306-1312.
46. Kuo, P., M. Weinfeld, and J. Loscalzo. 1990. Effect of membrane fatty acyl composition on LDL metabolism in HepG2 hepatocytes. Biochemistry. 29:6626-6632.
47. Madden, T. D., M. B. Bally, M. J. Hope, P. R. Cullis, H. P. Schieren, and A. S. Janoff. 1985. Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents. Biochim. Biophys. Acta Biomembr. 817:67-74.
48. Womersley, C., P. S. Uster, A. S. Rudolph, and J. H. Crowe. 1986. Inhibition of dehydration-induced fusion between liposomal membranes by carbohydrates as measured by fluorescence energy-transfer. Cryobiology. 23:245-255.
49. Hoekstra, F. A., W. F. Wolkers, J. Buitink, E. A. Golovina, J. H. Crowe, and L. M. Crowe. 1997. Membrane stabilization in the dry state. Comp. Biochem. Physiol. A. 117:335-341.
50. Richieri, G. V., A. Anel, and A. M. Kleinfeld. 1993. Interactions of long-chain fatty acids and albumin: determination of free fatty acid levels using the fluorescent probe ADIFAB. Biochemistry. 32:7574-7580.
51. Raz, A., and A. Livne. 1973. Differential effects of lipids on the osmotic fragility of erythrocytes. Biochim. Biophys. Acta. 311:222-229.
52. Massenburg, D., and B. R. Lentz. 1993. Poly(ethylene glycol)-induced fusion and rupture of dipalmitoylphosphatidylcholine large, unilamellar extruded vesicles. Biochemistry. 32:9172-9180.
53. Burgess, S. W., D. Massenburg, J. Yates, and B. R. Lentz. 1991. Poly(ethylene glycol)-induced lipid mixing but not fusion between synthetic phosphatidylcholine large unilamellar vesicles. Biochemistry. 30:4193-4200.
54. Crowe, J. H., B. D. McKersie, and L. M. Crowe. 1989. Effects of free fatty acids and transition temperature on the stability of dry liposomes. Biochim. Biophys. Acta Biomembr. 979:7-10.
55. Tieleman, D. P., and H. J. C. Berendsen. 1998. A molecular dynamics study of the pores formed by Escherichia coli OmpF porin in a fully hydrated palmitoyloleoylphosphatidylcholine bilayer. Biophys. J. 74:2786-2801.
56. Tieleman, D. P., L. R. Forrest, M. S. P. Sansom, and H. J. C. Berendsen. 1998. Lipid properties and the orientation of aromatic residues in OmpF, Influenza M2, and alamethicin systems: molecular dynamics simulations. Biochemistry. 37:17554-17561.
57. Leekumjorn, S., and A. K. Sum. 2007. Molecular characterization of gel and liquid-crystalline structures of fully hydrated POPC and POPE bilayers. J. Phys. Chem. B. 111:6026-6033.
58. Ryckaert, J. P., and A. Bellemans. 1975. Molecular dynamics of liquid normal-butane near its boiling-point. Chem. Phys. Lett. 30:123-125.
59. Berger, O., O. Edholm, and F. Jähnig. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72:2002-2013.
60. Jorgensen, W. L., and J. Tirado-Rives. 1988. The OPLS potential function for proteins. Energy minimizations for crystals of cyclic peptides and crambin. J. Am. Chem. Soc. 110:1657-1666.
61. Essex, J. W., M. M. Hann, and W. G. Richards. 1994. Molecular dynamics simulation of a hydrated phospholipid-bilayer. Philos. T. Roy. Soc. B. 344:239-260.
62. Chiu, S. W., M. Clark, V. Balaji, S. Subramaniam, H. L. Scott, and E. Jakobsson. 1995. Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane. Biophys. J. 69:1230-1245.
63. Damm, W., A. Frontera, J. Tirado-Rives, and W. L. Jorgensen. 1997. OPLS all-atom force field for carbohydrates. J. Comput. Chem. 18:1955-1970.
64. van Gunsteren, W. F., and H. J. C. Berendsen. 1987. GROMOS-87 Manual. Biomos BV, AG Groningen, Nijenborgh, The Netherlands.
65. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, J. Hermans, and B. Pullman. 1981. Intermolecular Forces. Reidel, Dordrecht, The Netherlands.
66. Leekumjorn, S., and A. K. Sum. 2006. Molecular simulation study of structural and dynamic properties of mixed DPPC/DPPE bilayers. Biophys. J. 90:3951-3965.
67. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: an N· log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
68. Essman, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
69. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91:43-56.
70. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
71. Virginia Tech. Terascale Computing Facility. http://www.tcf.vt.edu.
72. Sum, A. K., R. Faller, and J. J. de Pablo. 2003. Molecular simulation study of phospholipid bilayers and insights of the interactions with disaccharides. Biophys. J. 85:2830-2844.
73. Pereira, C. S., R. D. Lins, I. Chandrasekhar, L. C. G. Freitas, and P. H. Hünenberger. 2004. Interaction of the disaccharide trehalose with a phospholipid bilayer: a molecular dynamics study. Biophys. J. 86:2273-2285.
74. Villarreal, M. A., S. B. Díaz, E. A. Disalvo, and G. G. Montich. 2004. Molecular dynamics simulation study of the interaction of trehalose with lipid membranes. Langmuir. 20:7844-7851.
75. Doxastakis, M., A. K. Sum, and J. J. de Pablo. 2005. Modulating membrane properties: the effect of trehalose and cholesterol on a phospholipid bilayer. J. Phys. Chem. B. 109:24173-24181.
76. Pereira, C. S., and P. H. Hunenberger. 2006. Interaction of the sugars trehalose, maltose and glucose with a phospholipid bilayer: a comparative molecular dynamics study. J. Phys. Chem. B. 110:15572-15581.
77. Leekumjorn, S., and A. K. Sum. 2006. Molecular investigation of the interactions of trehalose with lipid bilayers of DPPC, DPPE and their mixture. Mol. Simul. 32:219-230.
78. Rudolph, A. S., and J. H. Crowe. 1985. Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology. 22:367-377.
79. 2 enzyme: a molecular dynamics simulation study. Biophys. J. 80:565-578.
80. Knecht, V., A. E. Mark, and S. J. Marrink. 2006. Phase behavior of a phospholipid/fatty acid/water mixture studied in atomic detail. J. Am. Chem. Soc. 128:2030-2034.
81. Eliasz, A. W., D. Chapman, and D. F. Ewing. 1976. Phospholipid phase transitions. Effects of n-alcohols, n-monocarboxylic acids, phenylalkyl alcohols and quaternary ammonium compounds. Biochim. Biophys. Acta. Biomembranes. 448:220-230.
82. Mabrey, S., and J. M. Sturtevant. 1977. Incorporation of saturated fatty acids into phosphatidylcholine bilayers. Biochim. Biophys. Acta Lipids Lipid Metabol. 486:444-450.
83. Brady, J. W., and R. K. Schmidt. 1993. The role of hydrogen bonding in carbohydrates: molecular dynamics simulations of maltose in aqueous solution. J. Phys. Chem. 97:958-966.
84. Skibinsky, A., R. M. Venable, and R. W. Pastor. 2005. A molecular dynamics study of the response of lipid bilayers and monolayers to trehalose. Biophys. J. 89:4111-4121.
85. Venable, R. M., A. Skibinsky, and R. W. Pastor. 2006. Constant surface tension molecular dynamics simulations of lipid bilayers with trehalose. Mol. Simul. 32:849-855.
86. Edholm, O., and J. F. Nagle. 2005. Areas of molecules in membranes consisting of mixtures. Biophys. J. 89:1827-1832.
87. König, B., U. Dietrich, and G. Klose. 1997. Hydration and structural properties of mixed lipid/surfactant model membranes. Langmuir. 13:525-532.
88. Rand, R. P., and V. A. Parsegian. 1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta Rev. Biomembranes. 988:351-376.
89. Shinoda, W., and S. Okazaki. 1998. A Voronoi analysis of lipid area fluctuation in a bilayer. J. Chem. Phys. 109:1517-1521.
90. Thilo, L., H. Trauble, and P. Overath. 1977. Mechanistic interpretation of influence of lipid phase-transitions on transport functions. Biochemistry. 16:1283-1290.
91. Welti, R., D. A. Rintoul, F. Goodsaid-Zalduondo, S. Felder, and D. F. Silbert. 1981. Gel phase phospholipid in the plasma membrane of sterol-depleted mouse LM cells. Analysis by fluorescence polarization and x-ray diffraction. J. Biol. Chem. 256:7528-7535.
92. Herreros, J., T. Ng, and G. Schiavo. 2001. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell. 12:2947-2960.
93. Fantini, J., N. Garmy, R. Mahfoud, and N. Yahi. 2002. Lipid rafts: structure, function and role in HIV, Alzheimer's and prion diseases. Expert Rev. Mol. Med. 2002:1-22.
94. Lafont, F., and F. G. van der Goot. 2005. Bacterial invasion via lipid rafts. Cell. Microbiol. 7:613-620.
95. Smondyrev, A. M., and M. L. Berkowitz. 1999. Molecular dynamics simulation of DPPC bilayer in DMSO. Biophys. J. 76:2472-2478.
96. Chiu, S. W., E. Jakobsson, and H. L. Scott. 2001. Combined Monte Carlo and molecular dynamics simulation of hydrated lipid-cholesterol lipid bilayers at low cholesterol concentration. Biophys. J. 80:1104-1114.
97. Róg, T., and M. Pasenkiewicz-Gierula. 2006. Cholesterol effects on a mixed-chain phosphatidylcholine bilayer: a molecular dynamics simulation study. Biochimie. 88:449-460.
98. Cournia, Z., G. M. Ullman, and J. C. Smith. 2007. Differential effects of cholesterol, ergosterol and lanosterol on a dipalmitoyl phosphatidylcholine membrane: a molecular dynamics simulation study. J. Phys. Chem. B. 111:1786-1801.
99. Unger, R. H., and Y. T. Zhou. 2001. Lipotoxicity of β-cells in obesity and in other causes of fatty acid spillover. Diabetes. 50(Suppl 1):S118-S121.
100. Awad, A. B., and A. A. Spector. 1976. Modification of the fatty acid composition of Ehrlich ascites tumor cell plasma membranes. Biochim. Biophys. Acta Biomembr. 426:723-731.
101. Burns, C. P., D. G. Luttenegger, D. T. Dudley, G. R. Buettner, and A. A. Spector. 1979. Effect of modification of plasma membrane fatty acid composition on fluidity and methotrexate transport in L1210 murine leukemia cells. Cancer Res. 39:1726-1732.
102. Girotti, A. W. 1998. Lipid hydroperoxide generation, turnover, and effector action in biological systems. J. Lipid Res. 39:1529-1542.
103. Aldini, G., P. Granata, M. Orioli, E. Santaniello, and M. Carini. 2003. Detoxification of 4-hydroxynonenal (HNE) in keratinocytes: characterization of conjugated metabolites by liquid chromatography/electrospray ionization tandem mass spectrometry. J. Mass Spectrom. 38:1160-1168.
104. Hoff, H. F., J. O'Neil, Z. P. Wu, G. Hoppe, and R. L. Salomon. 2003. Phospholipid hydroxyalkenals - biological and chemical properties of specific oxidized lipids present in atherosclerotic lesions. Arterioscler. Thromb. Vasc. 23:275-282.
105. Reis, A., M. R. Domingues, F. M. Amado, A. J. Ferrer-Correia, and P. Domingues. 2005. Separation of peroxidation products of diacylphosphatidylcholines by reversed-phase liquid chromatography-mass spectrometry. Biomed. Chromatogr. 19:129-137.
106. Chatterjee, S. N., and S. Agarwal. 1988. Liposomes as membrane model for study of lipid peroxidation. Free Radic. Biol. Med. 4:51-72.
107. Goldstein, R. M., and G. Weissmann. 1977. Effects of the generation of superoxide anion on permeability of liposomes. Biochem. Biophys. Res. Commun. 75:604-609.
108. Mandal, T. K., and S. N. Chatterjee. 1980. Ultraviolet- and sunlight-induced lipid peroxidation in liposomal membrane. Radiat. Res. 83:290-302.
109. Kunimoto, M., K. Inoue, and S. Nojima. 1981. Effect of ferrous ion and ascorbate-induced lipid peroxidation on liposomal membranes. Biochim. Biophys. Acta. 646:169-178.