Spin trapping and cytoprotective properties of fluorinated amphiphilic carrier conjugates of cyclic versus linear nitrones

Chemical Research in Toxicology

Volumn 22, Issue 9, 2009, Pages 1570-1581

  Durand, Grégory ^b   Prosak, Robert A ^a   Han, Yongbin ^a   Ortial, Stéphanie ^b   Rockenbauer, Antal ^c   Pucci, Bernard ^b   Villamena, Frederick A ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF AVIGNON   (France)

^c CHEMICAL RESEARCH CENTER   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

3 MORPHOLUNOSYNONIMINE HYDROCHLORIDE; 4 HYDROXYNONENAL; 5,5 DIMETHYL 1 PYRROLINE 1 OXIDE; AMPO; CARRIER PROTEIN; CHLORIDE; CYTOTOXIC AGENT; FAMPO; FAPBN; FLUORINATED AMPHIPHILIC CARRIER; FLUORINE; HYDROGEN PEROXIDE; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN INHIBITOR; NITRONE DERIVATIVE; PBN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; AORTA; ARTICLE; CELL DEATH; CELL PROTECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; DRUG STRUCTURE; DRUG SYNTHESIS; ENDOTHELIUM CELL; NONHUMAN; PHYSICAL CHEMISTRY; PROTEIN STABILITY; SPIN TRAPPING; SYNTHESIS;

ALDEHYDES; ANIMALS; ANTIHYPERTENSIVE AGENTS; CATTLE; CROSS-LINKING REAGENTS; DRUG CARRIERS; ENDOTHELIAL CELLS; FLUORINE; HYDROGEN PEROXIDE; MOLSIDOMINE; NITROGEN OXIDES; SPIN TRAPPING;

BOVINAE;

EID: 70349339630     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx900114v     Document Type: Article

References (81)

1. Nishikawa, T., Edelstein, D., Du, X. L., Yamagishi, S.-I., Matsumura, T., Kaneda, Y., Yorek, M. A., Beebe, D., Oates, P. J., Hammes, H.- P., Giardino, I., and Brownlee, M. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycemic damage. Nature 404, 787-791.
2. Nemoto, S., Takeda, K., Yu, Z.-X., Ferrans, V. J., and Finkel, T. (2000) Role for mitochondrial oxidants as regulators of cellular metabolism. Mol. Cell. Biol. 20, 7311-7318.
3. Gutierrez, J., Ballinger, S. W., Darley-Usmar, V. M., and Landar, A. (2006) Free radicals, mitochondria, and oxidized lipids. The emerging role in signal transduction in vascular cells. Circ. Res. 99, 924-932. (Pubitemid 44657795)
4. Dreher, D., and Junod, A. F. (1996) Role of oxygen free radicals in cancer development. Eur. J. Cancer 32A, 30-38. (Pubitemid 26086324)
5. Petrone, W. F., English, D. K., Wong, K., and McCord, J. M. (1980) Free radicals and inflammation: Superoxide-dependent activation of a neutrophil chemotactic factor in plasma. Proc. Natl. Acad. Sci. U.S.A. 77, 1159-1163. (Pubitemid 10105076)
6. Zweier, J. L., and Talukder, M. A. H. (2006) The role of oxidants and free radicals in reperfusion injury. Cardiovasc. Res. 70, 181-190.
7. Kaliora, A. C., Dedoussis, G. V. Z., and Schmidt, H. (2006) Dietary antioxidants in preventing atherogenesis. Atherosclerosis 187, 1-17.
8. Carr, A., and Frei, B. (2000) The role of natural antioxidants in preserving the biological activity of endothelium-derived nitric oxide. Free Radical Biol. Med. 28, 1806-1814. (Pubitemid 30628667)
9. Moosmann, B., and Behl, C. (2002) Antioxidants as treatment for neurodegenerative disorders. Expert Opin. Invest. Drugs 11, 1407-1435.
10. Villamena, F. A., and Zweier, J. L. (2004) Detection of reactive oxygen and nitrogen species by EPR spin trapping. Antioxid. Redox Signaling 6, 619-629. (Pubitemid 38625382)
11. Floyd, R. A., Kopke, R. D., Choi, C.-H., Foster, S. B., Doblas, S., and Towner, R. A. (2008) Nitrones as therapeutics. Free Radical Biol. Med. 45, 1361-1374.
12. Maples, K. R., Green, A. R., and Floyd, R. A. (2004) Nitrone-related therapeutics: potential of NXY-059 for the treatment of acute ischaemic stroke. CNS Drugs 18, 1071-1084. (Pubitemid 40007491)
13. Floyd, R. A., Hensley, K., Forster, M. J., Kelleher-Andersson, J. A., and Wood, P. L. (2002) Nitrones, their value as therapeutics and probes to understand aging. Mech. Ageing Dev. 123, 1021-1031. (Pubitemid 34603085)
14. Tosaki, A., Blasig, I. E., Pali, T., and Ebert, B. (1990) Heart protection and radical trapping by DMPO during reperfusion in isolated working rat hearts. Free Radical Biol. Med. 8, 363-372. (Pubitemid 20186983)
15. Zuo, L., Chen, Y. R., Reyes, L. A., Lee, H. L., Chen, C. L., Villamena, F. A., and Zweier, J. L. (2009) The radical trap 5,5-dimethyl-1- pyrroline N-oxide exerts dose-dependent protection against myocardial ischemia-reperfusion injury through preservation of mitochondrial electron transport J. Pharmacol. Exp. Ther. 329, 515-523.
16. Rosen, G. M. B., Bradley, E., Howard, J., and Pou, S. (1999) Free Radicals: Biology and Detection By Spin Trapping, Oxford University Press, New York.
17. Villamena, F. A., Xia, S., Merle, J. K., Lauricella, R., Tuccio, B., Hadad, C. M., and Zweier, J. L. (2007) Reactivity of superoxide radical anion with cyclic nitrones: role of intramolecular h-bond and electrostatic effects. J. Am. Chem. Soc. 129, 8177-8191. (Pubitemid 47035131)
18. Durand, G., Choteau, F., Pucci, B., and Villamena, F. A. (2008) Reactivity of superoxide radical anion and hydroperoxyl radical with alpha-phenyl-N-tert-butylnitrone (PBN) derivatives. J. Phys. Chem. A 112, 12498-12509.
19. Villamena, F. A., Hadad, C. M., and Zweier, J. L. (2005) Comparative DFT study of the spin trapping of methyl, mercapto, hydroperoxy, superoxide, and nitric oxide radicals by various substituted cyclic nitrones. J. Phys. Chem. A 109, 1662-1674.
20. Locigno, E. J., Zweier, J. L., and Villamena, F. A. (2005) Nitric oxide release from the unimolecular decomposition of the superoxide radical anion adduct of cyclic nitrones in aqueous medium. Org. Biomol. Chem. 3, 3220-3227.
21. Villamena, F. A., Locigno, E. J., Rockenbauer, A., Hadad, C. M., and Zweier, J. L. (2007) Theoretical and experimental studies of the spin trapping of inorganic radicals by 5,5-dimethyl-1-pyrroline N-oxide (DMPO). 2. Carbonate radical anion. J. Phys. Chem. A 111, 384-391. (Pubitemid 46278957)
22. Burgett, R. A., Bao, X., and Villamena, F. A. (2008) Superoxide radical anion adduct of 5,5-dimethyl-1-pyrroline N-oxide (DMPO). 3. Effect of mildly acidic pH on the thermodynamics and kinetics of adduct formation. J. Phys. Chem. A 112, 2447-2455.
23. Ortial, S., Durand, G., Poeggeler, B., Polidori, A., Pappolla, M. A., Boeker, J., Hardeland, R., and Pucci, B. (2006) Fluorinated amphiphilic amino acid derivatives as antioxidant carriers: A new class of protective agents. J. Med. Chem. 49, 2812-2820.
24. Ouari, O., Polidori, A., Pucci, B., Tordo, P., and Chalier, F. (1999) Synthesis of a glycolipidic amphiphilic nitrone as a new spin trap. J. Org. Chem. 64, 3554-3556. (Pubitemid 29232962)
25. Richard, C., Chaumet-Riffaud, P., Belland, A., Parat, A., Contino-Pepin, C., Bessodes, M., Scherman, D., Pucci, B., and Mignet, N. (2009) Amphiphilic perfluoroalkyled carbohydrates as new tools for liver imaging. Int. J. Pharm., in press, doi: 10.1016/j.ijpharm.2009.05.045.
26. Chabaud, E., Barthélémy, P., Mora, N., Popot, J. L., and Pucci, B. (1998) Stabilization of integral membrane proteins in aqueous solutions using fluorinated surfactants. Biochimie 80, 515-530. (Pubitemid 28425398)
27. Hsieh, K. H., Needleman, P., and Marshall, G. R. (1987) Long-acting angiotensin II inhibitors containing hexafluorovaline in position 8. J. Med. Chem. 30, 1097-1100. (Pubitemid 17120794)
28. Périno, S., Contino-Pépin, C., Jasseron, S., Rapp, M., Maurizis, J.-C., and Pucci, B. (2006) Design, synthesis and preliminary biological evaluations of novel amphiphilic drug carriers. Bioorg. Med. Chem. Lett. 16, 1111-1114. (Pubitemid 43142972)
29. Wolf, W., Presant, C. A., and Waluch, V. (2000) 19F-MRS studies of fluorinated drugs in humans. Adv. Drug Delivery Rev. 41, 55-74. (Pubitemid 30122949)
30. Asanuma, T., Yasui, H., Inanami, O., Waki, K., Takahashi, M., Iizuka, D., Uemura, T., Durand, G., Polidori, A., Kon, Y., Pucci, B., and Kuwabara, M. (2007) A new amphiphilic derivative, N-{[4-(lactobionamido) methyl]benzylidene}- 1,1-dimethyl-2-(octylsulfanyl)ethylamine N-oxide, has a protective effect against copper-induced fulminant hepatitis in long-evans cinnamon rats at an extremely low concentration compared with its original form alpha-phenyl-N- (tertbutyl) nitrone. Chem. Biodiversity 4, 2253-2267. (Pubitemid 47527676)
31. Durand, G., Poeggeler, B., Boeker, J., Raynal, S., Polidori, A., Pappolla, M. A., Hardeland, R., and Pucci, B. (2007) Fine-tuning the amphiphilicity: a crucial parameter in the design of potent alphaphenyl- N-tert-butylnitrone analogues. J. Med. Chem. 50, 3976-3979. (Pubitemid 47301730)
32. Durand, G., Polidori, A., Ouari, O., Tordo, P., Geromel, V., Rustin, P., and Pucci, B. (2003) Synthesis and preliminary biological evaluations of ionic and nonionic amphiphilic alpha-phenyl-N-tert-butylnitrone derivatives. J. Med. Chem. 46, 5230-5237. (Pubitemid 37414192)
33. Durand, G., Polidori, A., Salles, J.-P., and Pucci, B. (2003) Synthesis of a new family of glycolipidic nitrones as potential antioxidant drugs for neurodegenerative disorders. Bioorg. Med. Chem. Lett. 13, 859-862. (Pubitemid 36255554)
34. Poeggeler, B., Durand, G., Polidori, A., Pappolla, M. A., Vega-Naredo, I., Coto-Montes, A., Böker, J., Hardeland, R., and Pucci, B. (2005) Mitochondrial medicine: Neuroprotection and life extension by the new amphiphilic nitrone LPBNAH acting as a highly potent antioxidant agent. J. Neurochem. 95, 962-973. (Pubitemid 41713482)
35. Tanguy, S., Durand, G., Reboul, C., Polidori, A., Pucci, B., Dauzat, M., and Obert, P. (2006) Protection against reactive oxygen species injuries in rat isolated perfused hearts: Effect of LPBNAH, a new amphiphilic spin-trap derived from PBN. Cardiovasc. Drugs Ther. 20, 147-149. (Pubitemid 43876099)
36. Finkelstein, E., Rosen, G. M., and Rauckman, E. J. (1980) Spin trapping. Kinetics of the reaction of superoxide and hydroxyl radicals with nitrones. J. Am. Chem. Soc. 102, 4994-4999.
37. Frejaville, C., Karoui, H., Tuccio, B., le Moigne, F., Culcasi, M., Pietri, S., Lauricella, R., and Tordo, P. (1994) 5-Diethoxyphosphoryl-5- methyl-1-pyrroline N-oxide (DEPMPO): A new phosphorylated nitrone for the efficient in vitro and in vivo spin trapping of oxygen-centered radicals. J. Chem. Soc., Chem. Commun. 1793-1794.
38. Tsai, P., Elas, M., Parasca, A. D., Barth, E. D., Mailer, C., Halpern, H. J., and Rosen, G. M. (2001) 5-Carboxy-5-methyl-1-pyrroline N-oxide: A spin trap for the hydroxyl radical. J. Chem. Soc., Perkin Trans. 2, 875-880. (Pubitemid 33281706)
39. Halgren, T. A. (1996) Merck molecular force field. I. Basis, form, scope, parameterization and performance of MMFF94. J. Comput. Chem. 17, 490-519.
40. MacroModel 9.6 (2005) Schrödinger, LLC, New York, NY.
41. Still, W. C., Tempczyk, A., Hawley, R. C., and Hendrickson, T. (1990) Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112, 6127-6129.
42. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., 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, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2003) Gaussian 03, Gaussian, Inc, Pittsburgh PA.
43. Barone, V., Cossi, M., and Tomasi, J. (1997) A new definition of cavities for the computation of solvation free energies by the polarizable continuum model. J. Chem. Phys. 107, 3210-3221. (Pubitemid 127568937)
44. Barone, V., Cossi, M., and Tomasi, J. (1998) Geometry optimization of molecular structures in solution by the polarizable continuum model. J. Comput. Chem. 19, 404-417. (Pubitemid 128573764)
45. Cossi, M., Barone, V., Cammi, R., and Tomasi, J. (1996) Ab initio study of solvated molecules: Aa new implementation of the polarizable continuum model. Chem. Phys. Lett. 255, 327-335. (Pubitemid 126163033)
46. Tomasi, J., Mennucci, B., and Cammi, R. (2005) Quantum mechanical continuum solvation models. Chem. Rev. 105, 2999-3093. (Pubitemid 41222791)
47. Tomasi, J., and Persico, M. (1994) Molecular interactions in solution: an overview of methods based on continuous distributions of the solvent. Chem. Rev. 94, 2027-2094. (Pubitemid 124000195)
48. Rockenbauer, A., and Korecz, L. (1996) Automatic computer simulations of ESR spectra. Appl. Magn. Reson. 10, 29-43. (Pubitemid 126675693)
49. Ohlweiler, D. F., Taylor, V. L., and Schmidt, C. J. (1997) Radical trapping and inhibition of iron-dependent CNS damage by cyclic nitrone spin traps. J. Neurochem. 68, 1173-1182.
50. Kim, S., Vilela, G. V. M. A., Bouajila, J., Dias, A. G., Cyrino, F. Z. G. A., Bouskela, E., Costa, P. R. R., and Nepveu, F. (2007) [alpha]-Phenyl-N-tert- butyl nitrone (PBN) derivatives: Synthesis and protective action against microvascular damages induced by ischemia/ reperfusion. Bioorg. Med. Chem. 15, 3572-3578. (Pubitemid 46546634)
51. Janzen, E. G., West, M. S., Kotake, Y., and DuBose, C. M. (1996) Biological spin trapping methodology. III. Octanol-water partition coefficients of spin-trapping compounds. J. Biochem. Biophys. Meth. 32, 183-190. (Pubitemid 26238461)
52. Abla, M., Durand, G., and Pucci, B. (2008) Glucose-based surfactants with hydrogenated, fluorinated, or hemifluorinated tails: Synthesis and comparative physical-chemical characterization. J. Org. Chem. 73, 8142-8153.
53. Israelachvili, J. N. (1992) Intermolecular and Surface Forces, 2nd ed., Academic Press, San Diego, CA.
54. Nagarajan, R. (2002) Molecular packing parameter and surfactant self-assembly: The neglected role of the surfactant tail. Langmuir 18, 31-38.
55. Schneider, H.-J., Hacket, F., Ruediger, V., and Ikeda, H. (1998) NMR studies of cyclodextrins and cyclodextrin complexes. Chem. Rev. 98, 1755-1785. (Pubitemid 128633436)
56. Chalier, F., Ouari, O., and Tordo, P. (2004) ESR study of spin-trapping with two glycosylated analogues of PBN able to target cell membrane lectins. Org. Biomol. Chem. 2, 927-934.
57. Buettner, G. R. (1993) The pecking order of free radicals and antioxidants: Lipid peroxidation, alpha;-tocopherol and ascorbate. Arch. Biochem. Biophys. 300, 535-543. (Pubitemid 23232908)
58. Allouch, A., Lauricella, R. P., and Tuccio, B. N. (2007) Effect of pH on superoxide/hydroperoxyl radical trapping by nitrones: An EPR/ kinetic study. Mol. Phys. 105, 2017-2024.
59. Villamena, F. A., Merle, J. K., Hadad, C. M., and Zweier, J. L. (2007) Rate constants of hydroperoxyl radical addition to cyclic nitrones: A DFT study. J. Phys. Chem. A 111, 9995-10001.
60. Bienert, G. P., Moller, A. L., Kristiansen, K. A., Schulz, A., Moller, I. M., Schjoerring, J. K., and Jahn, T. P. (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183-1192. (Pubitemid 47076557)
61. Calamita, G., Ferri, D., Gena, P., Liquori, G. E., Cavalier, A., Thomas, D., and Svelto, M. (2005) The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water. J. Biol. Chem. 280, 17149-17153. (Pubitemid 41389180)
62. Ryter, S. W., Kim, H. P., Hoetzel, A., Park, J. W., Nakahira, K., Wang, X., and Choi, A. M. K. (2007) Mechanisms of cell death in oxidative stress. Antioxid. Redox Signaling 9, 49-89. (Pubitemid 44901874)
63. Joseph, J. A., Strain, J. G., Jimenez, N. D., and Fisher, D. (1997) Oxidant injury in PC12 cells-a possible model of calcium " dysregulation" in aging: I. Selectivity of protection against oxidative stress. J. Neurochem. 69, 1252-1258.
64. Floyd, R. A., and Hensley, K. (2000) Reactive Oxygen Species: Nitrone inhibition of age-associated oxidative damage. Ann. N.Y. Acad. Sci. 899, 222-237.
65. Chamulitrat, W., Parker, C. E., Tomer, K. B., and Mason, R. P. (1995) Phenyl N-tert-butyl nitrone forms nitric oxide as a result of its Fe(III)- catalyzed hydrolysis or hydroxyl radical adduct formation. Free Radical Res. 23, 1-14.
66. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624. (Pubitemid 20080360)
67. Ishii, M., Shimizu, S., Momose, K., and Yamamoto, T. (1999) SIN- 1-induced cytotoxicity in cultured endothelial cells involves reactive oxygen species and nitric oxide: protective effect of sepiapterin. J. Cardiovasc. Pharmacol. 33, 295-300. (Pubitemid 29066673)
68. Lomonosova, E. E., Kirsch, M., Rauen, U., and De Groot, H. (1998) The critical role of Hepes in SIN-1 cytotoxicity, peroxynitrite versus hydrogen peroxide. Free Radical Biol. Med. 24, 522-528. (Pubitemid 28150469)
69. Szabo, C., Ischiropoulos, H., and Radi, R. (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nature Rev. Drug Discovery 6, 662-680. (Pubitemid 47207751)
70. Ioannidis, l., and de Groot, H. (1993) Cytotoxicity of nitric oxide in Fu5 rat hepatoma cells: evidence for co-operative action with hydrogen peroxide. Biochem. J. 296, 341-345.
71. Trackey, J. L., Uliasz, T. F., and Hewett, S. J. (2001) SIN-1-induced cytotoxicity in mixed cortical cell culture: peroxynitrite-dependent and -independent induction of excitotoxic cell death. J. Neurochem. 79, 445-455.
72. Goldstein, S., Samuni, A., and Merenyi, G. (2004) Reactions of nitric oxide, peroxynitrite, and carbonate radicals with nitroxides and their corresponding oxoammonium cations. Chem. Res. Toxicol. 17, 250-257. (Pubitemid 38252505)
73. Goldstein, S., Samuni, A., and Russo, A. (2003) Reaction of cyclic nitroxides with nitrogen dioxide: the intermediacy of the oxoammonium cations. J. Am. Chem. Soc. 125, 8364-8370. (Pubitemid 36828600)
74. Samuni, A., Goldstein, S., Russo, A., Mitchell, J. B., Krishna, M. C., and Neta, P. (2002) Kinetics and mechanism of hydroxyl radical and OH-adduct radical reactions with nitroxides and with their hydroxylamines. J. Am. Chem. Soc. 124, 8719-8724. (Pubitemid 34791043)
75. Uchida, K. (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog. Lipid Res. 42, 318-343. (Pubitemid 36411689)
76. Whitsett, J., Picklo, M. J., Sr., and Vasquez-Vivar, J. (2007) 4-Hydroxy- 2-nonenal increases superoxide anion radical in endothelial cells via stimulated GTP cyclohydrolase proteasomal degradation. Arterioscler., Thromb., Vasc. Biol. 27, 2340-2347. (Pubitemid 350203948)
77. Fukuda, A., Osawa, T., Hitomi, K., and Uchida, K. (1996) 4-Hydroxy- 2-nonenal cytotoxicity in renal proximal tubular cells: protein modification and redox alteration. Arch. Biochem. Biophys. 333, 419-426. (Pubitemid 26304909)
78. Ishimura, A., Ishige, K., Taira, T., Shimba, S., Ono, S.-I., Ariga, H., Tezuka, M., and Ito, Y. (2008) Comparative study of hydrogen peroxide- and 4-hydroxy-2-nonenal-induced cell death in HT22 cells. Neurochem. Int. 52, 776-785.
79. Kokubo, J., Nagatani, N., Hiroki, K., Kuroiwa, K., Watanabe, N., and Arai, T. (2008) Mechanism of destruction of microtubule structures by 4-hydroxy-2-nonenal. Cell Struct. Funct. 33, 51-59. (Pubitemid 351860901)
80. Li, Y., Cao, Z., Zhu, H., and Trush, M. A. (2005) Differential roles of 3H-1,2-dithiole-3-thione-induced glutathione, glutathione S-transferase and aldose reductase in protecting against 4-hydroxy-2-nonenal toxicity in cultured cardiomyocytes. Arch. Biochem. Biophys. 439, 80-90. (Pubitemid 40826545)
81. Subramaniam, R., Koppal, T., Green, M., Yatin, S., Jordan, B., Drake, J., and Butterfield, D. A. (1998) The free radical antioxidant vitamin E protects cortical synaptosomal membranes from amyloid betapeptide(25-35) toxicity but not from hydroxynonenal toxicity: relevance to the free radical hypothesis of Alzheimer's disease. Neurochem. Res. 23, 1403-1410. (Pubitemid 28500760)